Insights Into Insecticide-Resistance Mechanisms in Invasive Species

TYPE Review
PUBLISHED 09 January 2023

DOI 10.3389/fphys.2022.1112278
Insights into insecticide-resistance

OPEN ACCESS mechanisms in invasive species:
EDITED BY
Xun Zhu,
Institute of Plant Protection (CAAS), China
Challenges and control strategies
REVIEWED BY
Xinzheng Huang, Junaid Ali Siddiqui 1,2,3, Ruidong Fan 1,2,3, Hira Naz 4,
China Agricultural University, China
Xiaolei Zhang,
Bamisope Steve Bamisile 5,6, Muhammad Hafeez 7,
Yangtze University, China Muhammad Imran Ghani 1,2,3, Yiming Wei 8, Yijuan Xu 5 and
*CORRESPONDENCE Xiaoyulong Chen 1,2,3,9*
Xiaoyulong Chen,
1
chenxiaoyulong@sina.cn College of Agriculture, College of Tobacco Science, Guizhou University, Guiyang, China, 2International
Jointed Institute of Plant Microbial Ecology and Resource Management in Guizhou University, Ministry of
SPECIALTY SECTION
Agriculture, China & China Association of Agricultural Science Societies, Guizhou University, Guiyang, China,
This article was submitted to Invertebrate 3
Guizhou-Europe Environmental Biotechnology and Agricultural Informatics Oversea Innovation Center in
Physiology,
Guizhou University, Guizhou Provincial Science and Technology Department, Guiyang, China, 4Research and
a section of the journal
Development Centre for Fine Chemicals, National Key Laboratory of Green Pesticides, Guizhou University,
Frontiers in Physiology
Guiyang, China, 5Department of Entomology, South China Agricultural University, Guangzhou, China, 6Henry
RECEIVED 30 November 2022 Fok School of Biology and Agriculture, Shaoguan University, Shaoguan, China, 7State Key Laboratory of Rice
ACCEPTED 21 December 2022 Biology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China, 8Guangxi Key Laboratory of Rice
PUBLISHED 09 January 2023 Genetics and Breeding, Guangxi Crop Genetic Improvement and Biotechnology Lab, Rice Research Institute,
Guangxi Academy of Agricultural Sciences, Nanning, China, 9College of Science, Tibet University, Lhasa,
CITATION China
Siddiqui JA, Fan R, Naz H, Bamisile BS,
Hafeez M, Ghani MI, Wei Y, Xu Y and
Chen X (2023), Insights into insecticide-
resistance mechanisms in invasive species:
Challenges and control strategies. Threatening the global community is a wide variety of potential threats, most notably
Front. Physiol. 13:1112278.
doi: 10.3389/fphys.2022.1112278 invasive pest species. Invasive pest species are non-native organisms that humans
have either accidentally or intentionally spread to new regions. One of the most
COPYRIGHT
© 2023 Siddiqui, Fan, Naz, Bamisile, effective and first lines of control strategies for controlling pests is the application of
Hafeez, Ghani, Wei, Xu and Chen. This is an insecticides. These toxic chemicals are employed to get rid of pests, but they pose
open-access article distributed under the
great risks to people, animals, and plants. Pesticides are heavily used in managing
terms of the Creative Commons
Attribution License (CC BY). The use, invasive pests in the current era. Due to the overuse of synthetic chemicals,
distribution or reproduction in other numerous invasive species have already developed resistance. The resistance
forums is permitted, provided the original
development is the main reason for the failure to manage the invasive species.
author(s) and the copyright owner(s) are
credited and that the original publication in Developing pesticide resistance management techniques necessitates a thorough
this journal is cited, in accordance with understanding of the mechanisms through which insects acquire insecticide
accepted academic practice. No use,
resistance. Insects use a variety of behavioral, biochemical, physiological, genetic,
distribution or reproduction is permitted
which does not comply with these terms. and metabolic methods to deal with toxic chemicals, which can lead to resistance
through continuous overexpression of detoxifying enzymes. An overabundance of
enzymes causes metabolic resistance, detoxifying pesticides and rendering them
ineffective against pests. A key factor in the development of metabolic resistance is
the amplification of certain metabolic enzymes, specifically esterases, Glutathione
S-transferase, Cytochromes p450 monooxygenase, and hydrolyses. Additionally,
insect guts offer unique habitats for microbial colonization, and gut bacteria may
serve their hosts a variety of useful services. Most importantly, the detoxification of
insecticides leads to resistance development. The complete knowledge of invasive
pest species and their mechanisms of resistance development could be very helpful
in coping with the challenges and effectively developing effective strategies for the
control of invasive species. Integrated Pest Management is particularly effective at
lowering the risk of chemical and environmental contaminants and the resulting
health issues, and it may also offer the most effective ways to control insect pests.
Frontiers in Physiology 01 frontiersin.org

Siddiqui et al. 10.3389/fphys.2022.1112278
KEYWORDS
biological invasion, insecticide resistance, biodiversity risk, exotic species, resistance

mechanisms
1 Introduction the current era. Consequently, one billion kilos of chemicals are used
annually to combat crop pests (Alavanja, 2009; Drees et al., 2013). In
Invasive species pose risks to human health, food security, the several countries, pesticide usage has increased, i.e., Britain
survival of endangered species, economic loss, and ecosystem stability (18,000 tons), Italy (62,000 tons), Germany (4,800 tons), Poland
(Venette et al., 2021). Invasive pest species are also known by the (2,400 tons), and China (273,375 tons) (FAOSTAT Food and
names non-native, exotic, non-indigenous, and introduced. The Agriculture Organization of the United Nations, 2020). Despite
human race is responsible for its introduction, whether on purpose, their effectiveness, synthetic pesticides have raised questions about
by accident, or through trade. Besides the obvious danger to resistance to pests, environmental degradation, and potential health
biodiversity, these introduced species also pose a significant risk to impacts are all reasonable concerns (Du et al., 2020).
national biosecurity (Rao et al., 2018; Raghuteja et al., 2022). Species Insecticides are used to eliminate pests and disease-carrying
can now be transported to new regions of the world at an insects in farming. Several insecticides, including
extraordinary pace due to the rapid expansion of the world’s organophosphates, pyrethroids, and neonicotinoids, play pivotal
commercial and social networking. Awareness of the negative roles in pest management (Abdulahi et al., 2011). One of the most
effects of invasive species on local biodiversity and the resulting prominent examples of micro-evolution is the development of pest
economic loss in many nations has grown over the past resistance due to the widespread usage of insecticides. More than
two decades (Pimentel et al., 2005; Zhang et al., 2022). Recent 500 distinct pest species have been documented as having developed
research into the evolutionary genetics of invasive species has resistance to insecticides, according to previous research (Connor
found that the ability to adapt to natural selection may be more et al., 2011). Numerous pests, like corn earthworms and others, feed on
important for the successful invasion of some introduced species than a wide variety of crops around the world (cotton, peanuts, tobacco,
widespread physiological plasticity or tolerance. Therefore, it can etc.) and have developed resistance to insecticides. Several elements,
unintentionally boost the invasive species’ evolutionary potential biological, genetic, and operational, contribute to the emergence of
and enable its quick growth and geographical distribution in the resistance, but genetic aspects are regarded as the most helpful
area of introduction (Lavergne and Molofsky, 2007; Marbuah et al., (Karaağaç, 2012). However, future populations showing increasing
2014; Siddiqui et al., 2021; Venette et al., 2021; Hafeez et al., 2022b). insecticide resistance make pest control more difficult (Stratonovitch
As arthropods spread outside of their natural habitats, they meet et al., 2014). Insects have been found to use a variety of molecular
naïve animals and host plants as well as population-controlling resistance mechanisms, including metabolic and target sites.
pathogens, parasitoids, and predators. Opportunities to dominate Understanding species-level worldwide patterns are also helpful
and modify invaded areas arise when antagonistic and from a biosecurity aspect. Resistance-containing species pose a
coevolutionary relationships among invasive species are disrupted. significant concern as intruders as they can build new populations
The first introduction of invasive species (Grape phylloxera pest, that are already evolved to insecticidal stress. Invasive populations of
Daktulosphaira vitifoliae) was reported in Europe about the middle the Silverleaf white fly, Bemisia tabaci, are just one example of a
of the 19th century. At the same time, the emerald ash borer, Agrilus historical problem in Australia (Thia et al., 2021). Similarly, after the
planipennis, landed in North America and Europe in the early introduction of western flower thrips, Franklieniella occidentalis, into
twenties. The fall armyworm, Spodoptera frugiperda, devours maize Australia, many of the chemical pesticides used were ineffective
in Africa, causing a direct impact on food or the environment (Sileshi against the insect (Reitz and Funderburk, 2012). However,
et al., 2019), Darwin’s finches in the Galapagos were under attack by numerous urban pests are resistant to pesticides (e.g., cockroaches,
invading flies (Philornis downsi) (Fessl and Tebbich, 2002; Koop et al., houseflies, mosquitoes, ants, wasps, and termites) (Acevedo et al.,
2021), or red turpentine beetle (Dendroctonus valens) has a 2009; Liu, 2015; Mahapatro, 2017; Fardisi et al., 2019). Even though
devastating effect on China’s pine forests (Sun et al., 2013). insects can negatively affect agriculture, public health, and the
Indirect effects can be more subtle, such as when the brown environment, effective methods of controlling them are lacking
marmorated stink bug (Halyomorpha halys) spreads an aflatoxin- (Hardy, 2014).
producing fungus in the United States (Opoku et al., 2019), or In South Cumulative global knowledge of resistance mechanisms helps
America, dengue fever is spread by the Asian tiger mosquito (Aedes develop hypotheses and expectations at more localized scales. The
albopictus) (Ricas Rezende et al., 2020), and Xylella fastidiosa, a non- current review literature beam spotlights available knowledge on
native bacteria, is spread via spittlebugs (Occhibove et al., 2020). invasive species and broadly expands on the various species that
Indirect consequences on water, health, and the environment may have been documented to develop a broad spectrum of resistance
result from measures taken in response to arthropod invasions, against various classes of chemical insecticides. Moreover, possible
particularly if widespread use of pesticides is required (Milano and mechanisms of insecticide resistance in invasive species, their
Chèvre, 2019). management strategies, and future implication are also discussed.
Each year, the world’s food supply faces a 10%–30% loss due to
insect pests (Oerke, 2006) and exotic species-related damages worth
$20 billion (Pimentel et al., 2000). That is why it is so important to 2 Resistance in invasive insects
keep the pests that have affected our economy under control (Savary
et al., 2012). Insecticide use is thought to be the most effective pest Pesticide-induced resistance is defined as a heritable modification
control technique. Pesticides are heavily used in managing the pest in in a pest population’s sensitivity to pesticides, as evident in the

TABLE 1 A list of insecticide-resistant invasive species of China.
Scientific name Common Resistance against insecticide Country References

names
Aedes albopictus Asian tiger; mosquito Pyrethroid; Fenthion; Glyphosate; deltamethrin China Hou et al. (2020); Chen et al. (2018)
Bactrocera cucurbitae Dacus cucurbitae Organophosphorus; pyrethroid China Gu et al. (2015)
Bactrocera dorsalis Oriental fruit fly Malathion; Beta-cypermethrin, cyhalothrin China Wang et al. (2011); Chen et al. (2015)
Bemisia tabaci Cotton white fly Bifenthrin; thiamethoxam; acetamiprid; imidacloprid; chlorpyrifos China Qiu et al. (2009); Wang et al. (2011); Yang
et al. (2014)
Blattella germanica German cockroach Organophosphorus; DDVP; fenitrothion; diazinon; China Pai et al. (2005)
pirimiphosmethyl; chlopyrifos; propoxur; bendiocarb
Cydia pomonella Codling moth Chlorpyrifos; carbaryl China
Eriosoma lanigerum Woolly apple aphid imidacloprid China Jing et al. (2016)
Frankliniella Western flower Cyhalothrin; spinosad China Wang et al. (2011); Wang et al. (2014)
occidentalis thrips
Leptinotarsa Potato beetle Neonicotinoid China Liu et al. (2011); Xiong et al. (2010)
decemlineata
Liriomyza sativae Vegetable leaf miner Chlorpyrifos China Yan et al. (1998)
Lissorhoptrus Rice water weevil Chlorphenamide China Liu et al. (2018)

oryzophilus
Pectinophora Pink bollworm Decamethrin China Li et al. (1995)

gossypiella
Periplaneta American cockroach Neonicotinoid China Zhang et al. (2018)

americana
Solenopsis invicta Red imported fire ant Fipronil, beta-cypermethrin, indoxacarb China Siddiqui et al. (2022, 2022a)
Spodoptera fall armyworm Indoxacarb China Hafeez et al. (2021, 2022a)

frugiperda
Trialeurodes Greenhouse whitefly Malathion; glyphosate; deltamethrin; neonicotinoid; pyrethroids China Zhang et al. (1980); Liu et al. (2005)
vaporariorum
Thrips palmi Melon thrips Organochlorine; Organophosphorus; Pyrethroids China Zhao et al. (1995); Immaraju et al. (1992);
Broadbent and Pree (1997)
Trogoderma khapra beetle Phosphine China Borah et al. (1981)

granarium
repeated failure of the treated chemical products to achieve the 4) Target-site resistance
required control (Mahapatro, 2017). Resistance studies are essential 5) Metabolic resistance
in developing strategies for resistance mitigation and reducing possible 6) Resistance-inducing operational factors
insect pest outbreaks. A large number of invasive insect species have
been examined and found to exhibit resistance to various classes of 2.1.1 Behavioral resistance
insecticides in China (Table 1), and in some other parts of the world In the very first line of protection, organisms might develop
(Table 2). strategies to lessen their exposure to the uptake of a pesticide
(Dunlop et al., 2018; Lushchak et al., 2018). Insects can develop
resistance to chemicals through a number of different mechanisms,
2.1. Mechanism of insecticide resistance but an early and important one is a behavior response (Nansen et al.,
2016) (Figure 1). When exposed to a lethal toxin, insects may often
There is various mechanism mediating insecticide resistance cease feeding and may even leave the treated area by simply moving
development in insects. The major factors are behavioral resistance, from one field to another or into a deeper crop canopy (De Roode and
fitness cost, reduced penetration, target resistance, and metabolic Lefèvre, 2012; IRAC, 2022).
resistance. The mechanism underlying insecticide resistance in Behavioral resistance was well defined in a previous study by Sparks
insects can generally be categorized as follows. et al. (1989) as “evolved behavior that reduces an insect’s exposure to toxic
compounds or that allows an insect to survive in what would otherwise be a
1) Behavioral resistance toxic and fatal environment”. To survive, arthropod pests use behavioral
2) Fitness cost processes, which involve shifts in behavior and stay away from areas that
3) Penetration resistance have been sprayed with insecticides (Sparks et al., 1989). Insect movement

TABLE 2 A list of insecticide-resistant invasive species in the world.
Scientific name Common Resistance against Country References

names insecticide
Bactrocera dorsalis Oriental fruit fly Organophosphorus Pakistan Khan and Akram (2018); Hsu et al. (2004); Vontas et al. (2011)
Carbamates Taiwan Khan and Akram (2018); Hsu et al. (2004); Vontas et al. (2011)
Pyrethroid,; spinosad; Trichlorfon unknown Khan and Akram (2018); Hsu et al. (2004); Vontas et al. (2011)
Bemisia tabaci Cotton white fly Parathion-methyl; endosulfan America Byrne and Devonshire (1993)
Imidacloprid Europe Wang et al. (2011)
Cydia pomonella Codling moth Arsenate; DDT; organophosphorus; America Hough (1928); Cutright (1954); Moffit et al. (1988); Welter et al.
benzoyl urea (1991)
Decamethrin; abamectin France Bouvier et al. (1998); Reyes and Sauphanor (2008)
Glutathion; Chlopyrifos; Phosalone Spanish Rodríguez et al. (2010)
Frankliniella Western flower Carbamates (Methiocarb, Australia Martin and Workman (1994); Espinosa et al. (2002); Herron and
occidentalis thrips Bendiocarb) James (2005); Götte and Rybak (2011)
Organochlorine New Zealand Martin and Workman (1994); Espinosa et al. (2002); Herron and
James (2005); Götte and Rybak (2011)
Organophosphorus Spain Martin and Workman (1994); Espinosa et al. (2002); Herron and
James (2005); Götte and Rybak (2011)
Pyrethroid (fenvalerate) United States of Martin and Workman (1994); Espinosa et al. (2002); Herron and
America James (2005); Götte and Rybak (2011)
Leptinotarsa Potato beetle Carbofuran; pyrethroid Canada Harris and Svec (1981)
decemlineata
Periplaneta Americana Imidacloprid America Wang et al., 2004,2006; Ko et al., 2016

americana cockroach
Blattella germanica German cockroach Fipronil America Wang et al., 2004,2006; Ko et al., 2016
Periplaneta Australian Abamectin America Wang et al., 2004,2006; Ko et al., 2016

australasiae cockroach
Spodoptera fall armyworm Cyhalothrin; flubendiamide; America Gutiérrez-Moreno et al. (2019); Yu (1991)
frugiperda chlorantraniliprole
Thrips palmi Melon thrips Organochlorine; Organophosphorus America Zhao et al. (1995); Immaraju et al. (1992); Broadbent and Pree (1997)
Pyrethroids Canada Zhao et al. (1995); Immaraju et al. (1992); Broadbent and Pree (1997)
TABLE 3 Insecticide classification based on target site.
Chemical group Insecticide Target site

Organochlorines chlordane, dieldrin, DDT, lindane, methoxychlor, kepone, toxaphene, mirex, and benzene hexachloride GABA- gated chloride channel blocker
Organophosphates Azinphos-methyl, azamethiphos, fenitrothion, diazinon, dichlorvos, phosmet, parathion, tetrachlorvinphos, Acetylcholinesterase (AchE) inhibitors
malathion, methyl parathion, chlorpyrifos, terbufos
Carbamates Aldicarb, fenobucarb, oxamyl, carbofuran, ethienocarb, carbaryl, and methomyl Acetylcholinesterase (AchE) inhibitors
Pyrethroids alpha-cypermethrin, deltamethrin, and permethrin Sodium channel modulators (Nav)

Pyrethroids
See http://www.irac-online.org/modes-of-action/
can have a significant effect on the growth of insecticide resistance. resistance. For instance, the Colorado potato beetle (Leptinotarsa
Movement characteristics of an insect cannot determine the extent of decemlineata) has limited flight capabilities, so pockets of insecticide
insecticide exposure, impacting the selection pressure on the insect resistance have developed in growing regions across North America
population. It can also determine the degree to which insect populations (Alyokhin et al., 2008). For instance, Plutella xylostella Linnaeus, an
mix in the ecosystem, thus affecting the ability of resistant ales to increase in invasive species, has developed behavioral resistance by using site

FIGURE 1
Schematic diagram of the biological and behavioral mechanisms of insecticide resistance in invasive insects.
selection for egg laying in adults and larval mobility variations to escape toxin transmission (Theis et al., 2015). Moreover, the effective waste
lethal dosages of foliar-applied insecticides in the field (Sarfraz et al., 2005; removal of unhealthy materials (including dead ants). The ants
Zago et al., 2014). da Silva Nunes et al. (2020) found variation in the regularly clean and disinfect each other and the infected ants they
locomotor activity of P. xylostella adults between laboratory and field- come into contact with (Pull et al., 2018). Examples of behavioral
collected samples. Insects collected from the field exhibited elevated activity resistance occurred in recent studies, Wen et al. (2020) reported that
and decreased resting time compared to controls, suggesting that they were invasive fire ant (Solenopsis invicta) deposited soil particles on the
motivated to escape from treated surfaces. Host plant evasion may have ant replant to avoid contact. To minimize pesticide contact, another
resistance traits, such as producing more eggs or preferring to oviposit on study found that RIFA carried debris particles to cover the
plants with less hairy and delicate cuticles, as evidenced by research pesticide-treated region (Wen et al., 2021). When social ants
demonstrating these insects have evolved to avoid insecticides (Silva and come into touch with previously immunized nestmates, their
Furlong, 2012; Ang et al., 2014). Some other insects, such as female sheep ability to resist infection significantly improves (Konrad et al.,
blowflies (Lucillia cuprina), developed the ability to delay ovulation in the 2018). This social transfer of infection resistance could explain
presence of a pesticide intended for their larvae (Mariath et al., 1990). how colony members’ survival rates are raised due to group life,
Red Imported Fire Ants (RIFA) are the best example of despite the higher risks of transmission of alien agents (pesticides)
behavioral resistance because their excellent social system that occur (Traniello et al., 2002). Pesticide resistance has been
benefits their success (Dhami and Booth, 2008; Bertelsmeier recently found in RIFA, which might be the reason for the inability
et al., 2017; Jones and Robinson, 2018; Giraldo et al., 2021). to manage urban invasive ant species (Allen et al., 2018). The
Various behaviors play a role in developing resistance in RIFA, ineffectiveness of numerous biological and chemical control
such as antibiotic secretions and adaptive immunological responses programs to control the invasive species could be attributed to a
of colony members (Wilson-Rich et al., 2009), self- and mutual lack of understanding of ant behavior and the habits mentioned
grooming by ant nestmates can restrict or accelerate infection and above, among several other factors.

2.1.2 Fitness cost increase is the rate that an insect population will increase without
2.1.2.1 Biological resistance external constraints. When populations are affected by biological or
The biological and ecological factors discussed here constantly environmental constraints, the growth rate slows as it approaches a
interact to impact the risk of resistance development. Life cycle and carrying capacity (large population size that is sustainable) (Holt,
population factors are important biological parameters. 2009). Insect populations are regulated by multiple factors, e.g.,
Life cycle: An overriding aspect of insect biology that impacts an environmental conditions, host quality, and natural enemies. In the
insect’s ecological interactions and the development of pesticide example shown, insect predator populations lag behind prey
resistance is the insect’s life cycle (Sudo et al., 2018). Through a populations, but prey population decline after predator populations
pest’s life cycle, there are changing interactions with its host and build up (Culshaw-Maurer et al., 2020). The invasive insects invade a
environment. Optimal resistance management practices rely on an new place where they do not have a natural enemy, and the
understanding of these interactions. The life cycle of the insect pest is environmental condition is suitable for their survival, consequently,
the primary factor affecting the development of insecticide resistance; reasons for their success. For example, Solenopsis invicta invades many
in particular, the long life processes in bugs (Saulich, 2010) and short countries, can increase their population, and dominates the local fauna
life cycle with the abundant progeny of mosquitoes which has all the (Morrison et al., 2004; Siddiqui et al., 2021) (Figure 1).
properties suitable to swiftly developing resistance (Karunamoorthi Generation time is also important in the time required for
and Sabesan, 2013). individuals to complete their life cycle. This ranges from multiple
The insects have different reproductive phases that influence years per life cycle, as in the case of large pine weevil (Hylobius abietis)
resistance development through behavioral and genetic effects. (Inward et al., 2012), to numerous life cycles per year in Mosquitoes
Moreover, some ecological factors, such as environmental or host (Mendoza, 2016). This allows for more genetic recombination,
quality, will affect the reproduction phase (Helps et al., 2017). Most increasing genetic diversity and the probability of selecting resistant
insects undergo sexual reproduction, involving a male and female alleles. The population with multiple generations per year would more
union, and the resulting genetic recombination increases the genetic likely develop resistance to a pesticide because there would be more
variability in a population. For example, sexual reproduction in two- selection cycles (chances) to select for or to raise the percentage of
spotted spider mites (Tetranychus urticae) enhanced the genetic resistant ones in the final population. For example, mosquitoes have
variability in its population. It allowed for an increased potential multiple generations in short periods, which increases the possibility
for the development of resistance (Sun J. et al., 2022). On the other of the transfer of resistance alleles to the next generations and
hand, asexual reproduction involves no male-female union, with the increases their genetic diversity, leading to the resistant generation
best example found in aphids (Stöck et al., 2021) (Figure 1). This will (Mendoza, 2016). Another invasive species, Diamondback moths, can
increase the reproduction rate, but it will also limit the genetic undergo multiple generations annually, increasing the potential for
variability in a population. Multiple generations of asexually selection pressure across the population (Kliot and Ghanim, 2012)
reproducing aphids, such as the green peach aphid (Myzus persicae (Figure 1).
Sulzer), are produced each year. Still, only a single sexual generation is
likely to occur (Guillemaud et al., 2003). Among these reproductive 2.1.3 Penetration resistance
phases, the insects undergo the development phase, which is a The insect cuticle comprises two major layers of polysaccharide
maturation process. Organisms vary a great deal in how these chitin, lipids, and proteins. The chitin is in the inner procuticle, but
occur. Selection pressure can often occur throughout this life cycle there is no chitin in the thin outer epicuticles (Bass and Jones,
phase. For example, the Housefly goes through distinct development 2016). By coating cuticular hydrocarbons (CHCs) generated in
stages (e.g., egg, pupa, adult fly) as it grows (de Jonge et al., 2020). particular secretory cells in the epidermis called oenocytes on their
Moreover, the sweet potato white fly, B. tabaci, has been shown to be epicuticle, insects are able to protect themselves from drying out
resistant to neonicotinoids. The effects of thiamethoxam resistance (Falcon et al., 2019). Penetration resistance occurs when insects
selection on the life histories of B. tabaci B-biotype strains were slow down the engagement of xenobiotics within their bodies.
studied by comparing those of selected and non-selected strains Insects create barriers against the product using their outer
over multiple generations (Feng et al., 2009). The resistant cuticle, which protects them against a wide spectrum of
individuals had shorter life spans and lower fecundity than the insecticides (Figure 2) (Tangtrakulwanich and Reddy, 2014;
susceptible unselected strain. On the other hand, the nymphal Balabanidou et al., 2016). Because of this slowing process,
stages took longer to mature in the resistant strain. Further insecticides may take significantly longer to reach their protein
phenotypic changes were seen in the resistant strain, with reduced targets in neuronal cells (Fang et al., 2015). Scanning electron
body size across all instars and pupal stages compared to the microscopy indicated that resistant mosquitos have significantly
susceptible strain (Feng et al., 2009). So, the life span of the insect increased cuticle thickness, with the outer epicuticle accounting for
pest, its reproductive capacity, and its surrounding habitat are crucial much of the entire difference in whole cuticle thickness
elements in the evolution of resistance (Naqqash et al., 2016). An (Balabanidou et al., 2016). Some adaptations known as
insect’s lifecycle and developmental period play a crucial part in the penetration mechanisms slow the rate at which a pesticide is
growth of insecticide resistance (Figure 1). absorbed through the cuticle (Gunning et al., 1991; Ahmad
Population growth: The growth of insect populations influences et al., 2006). Evidence of penetration experimentation is
resistance development by determining the most successful frequently used to infer resistance (Ahmad et al., 2006; Puinean
individuals. Intense selection pressures from insecticide use, short et al., 2010); however, in order to distinguish expression differences
generation time, and readily available host crops have resulted in in cuticle-related genes between resistant and susceptible strains,
diamondback moth (P. xylostella) resistance to almost all groups of transcriptomics has also been applied (Thia et al., 2021). However,
insecticides (Taha, 2022; Venkatesan et al., 2022). The intrinsic rate of minimal studies on cuticular resistance in invasive insects such as

FIGURE 2
A schematic diagram represents the role of enzymes and gut microbiota in pesticide detoxification in invasive ants.
P. xylostella revealed a significant difference in cuticular et al., 2022). Comparing the amount of pesticide taken over time by
microRNAs between the chlorantraniliprole resistance resistant and susceptible types of insects is the simplest technique to
population and the susceptible population. They give insight calculate the penetration rate. Although, even a slight reduction in
into cuticular alteration during the development of resistance penetration might contribute significantly to the invasive insect
(Zhu et al., 2017; Shabbir et al., 2021). There is evidence of developing resistance to the insecticide (Venkatesan et al., 2022).
cuticular resistance in H. armigera, which successfully prevented
deltamethrin adsorption in the body by generating thicker cuticles 2.1.4 Target-site resistance
in resistant individuals compared to susceptible individuals, where Insecticides are chemicals (synthetic compounds or direct biological
insecticide percolation was substantially higher (Ahmad et al., materials) used to control insect pests (Wojciechowska et al., 2016).
2006). According to one study on Amyelois transitella However, the most successful synthetic insecticides are neuro-inhibitors
(Lepidoptera: Pyralidae), when an insect is repeatedly subjected (Figure 2). Despite the increasing cost and the risk of environmental
to pesticide pressure, the hydrocarbon profile in the cuticle tends to contamination, these are the world’s most widely used agents of insect
change, which may help to build cuticular resistance (Ngumbi pest control today (Yadav et al., 2022). Our study mainly discussed
et al., 2020). commonly used four classes of organic or synthetic pesticides, and they
Thickening or altering the chemical makeup of the insect cuticle are as follows: organochlorines, organophosphates (OPs), carbamates,
reduces toxicant uptake. A similar mechanism was observed in OP- and pyrethroids (Table 3). All of these pesticides target the insect’s central
resistant strains of Culex tarsalis (Whyard et al., 1994) and C. nervous system. For organochlorines, the neurological system is the
quinquefasciatus (Gong et al., 2022). The variation in pesticide primary target. The inhibitory neurotransmitter gamma-aminobutyric
transport across the cuticle of houseflies (Musca domestica acid (GABA) attaches to a specific type of chloride channel called a
Linnaeus) was also demonstrated (Malik et al., 2007). Similarly, GABA-gated chloride channel, and blocking these channels leads to
organophosphates, methyl carbamates, pyrethroids, and increased excitability in neurons (Al-Kuraishy et al., 2022). The
neonicotinoids resistance in Tribolium castaneum (Rösner et al., enzyme that breaks down acetylcholine, a neurotransmitter, is the
2020), OP resistance in Colorado potato beetle (Lepinotarsa target of carbamates and OPs. Other organochlorines and pyrethroids
decemilineata) (Yoon et al., 2022), and fenvalerate resistance in P. inhibit nerve impulse transmission by binding to and blocking the
xylostella (Mubashir and Seram, 2022), have all been confirmed to be function of Nat channel proteins in the neuron membrane (Lopez-
partly due to reduced penetration (Figure 2). This mechanism confers Suarez et al., 2022). Pyrethroids affect the sodium channels and lead
low levels (less than 5 - fold) of resistance and only becomes important to paralysis of the organism. When they attach to sodium channels, they
when combined with other resistant mechanisms. On the other hand, trigger excitatory paralysis and eventually death in insects (Davies et al.,
it appears to shield several different classes of pesticides (Venkatesan 2007).

Biologically modified insects may be resistant to insecticides “detoxification” (Jaffar et al., 2022). Metabolic resistance is of huge
because they have been altered genetically to inhibit the insecticide importance and is also one of the most studied mechanisms in insects.
from binding or interacting at its site of action (Fenibo et al., 2022). Insects use their enzymatic systems to digest pesticides, and resistant
The second most researched resistance mechanism in a wide variety of populations may have more of these enzymes or enzymes with
insects is target site insensitivity. As a result of changes in the target improved detoxifying capabilities (Karunaratne and Surendran,
site’s structure or accessibility, toxicants may no longer form stable 2022). Furthermore, to become more effective, these enzyme
bonds with them, a phenomenon known as target-site insensitivity systems may also be able to break down many different types of
(Venkatesan et al., 2022). Aphids have developed a resistance to pesticides (Vyas et al., 2022). Detoxifying enzymes enhance and
pyrethroids by developing resistance at the target site (knockdown accelerate the drug resistance caused by the metabolism of
resistance-kdr) (Valmorbida et al., 2022). insecticides (Siddiqui et al., 2022c; Siddiqui et al., 2022b). The
There are four major types of target sites such as 1) The over-produced enzymes in pests can develop protection against
insensitivity of acetylcholine esterase (AChE) has been identified as insecticides (Figure 2) (Rane et al., 2016; Khan et al., 2020).
an essential mechanism for pesticide resistance in numerous
agricultural insect pests to carbamates and organophosphates 2.1.5.1 Carboxylesterases (CarEs)
(Renault et al., 2022). Esterases are a diverse family of enzymes Carboxylesterases (CarEs) are an adaptable class of lipolytic
responsible for breaking down a wide range of ester bonds in both enzymes that catalyze the hydrolysis of esters into alcohol and acid
endogenous and exogenous substrates (Memarizadeh et al., 2011) and molecules. Widespread biocatalysis, drug metabolism, and endobiotic
play important roles in the insect’s ability to eliminate the toxic effects and xenobiotic degradation rely on these enzymes (Sood et al., 2016).
of insecticides. The enzyme acetylcholinesterase (AChE) is the target CarEs enzymes also detoxify environmental toxicants such as
of both organophosphate and carbamate insecticides because of its pyrethroids, a major insecticide class used worldwide (Staudinger
central role in the nervous system in hydrolyzing cholinergic et al., 2010). Recent studies on invasive species indicated that a
neurotransmitters and terminating nerve impulses (Devrnja et al., greater AChE and CarE esterase activity was seen in resistant
2022). Neonicotinoids, organophosphates, and methyl carbamates act populations compared to vulnerable ones such as S. invicta
as acetylcholinesterase inhibitors or as nicotinic acetylcholine receptor (Siddiqui et al., 2022b; 2022c), H. armigera (Young et al., 2005;
agonists (Devrnja et al., 2022). Prior to inhibiting acetylcholinesterase Wu et al., 2011), C. tarsalis (Whyard et al., 1994), and Aonidiella
(AChE), organophosphorus insecticides must be transformed into aurantia (Grafton-Cardwell et al., 2004) (Figure 2).
their oxon analogs by monooxygenases (Lorke and Petroianu, 2019) Biochemical methods using S. litura resistant strains from Korea
(Figure 2). 2) Sodium channel blocker insecticides (SCBIs) are a and India have shown the role of acetylcholinesterases in pesticide
relatively new group of pesticides exemplified by metaflumizone resistance (Yonggyun et al., 1998; Kranthi et al., 2002; Muthusamy
and indoxacarb, which are commercially registered chemicals. It is et al., 2011). In the same way, a carbamate-resistant strain of S. exigua
well-known that SCBIs like pyrethroids and DDT intoxicate insects by from California had an AChE enzyme that was about 30 times less
blocking their access to voltage-gated sodium channels (VGSCs) sensitive to methomyl than the enzyme from a sensitive laboratory
(Cens et al., 2022). The sodium channel in nerve cells is disrupted strain (Byrne and Toscano, 2001). However, molecular information
by KDR (knockdown resistance). This mechanism is widely exploited on the AChE point mutation exists for a number of species of
in pyrethroid and DDT resistance. Kdr and super kdr are the results of Spodoptera, while it is mostly available for S. frugiperda. When
a number of different mutations (Sun H. et al., 2022). 3) For insects, comparing two strains of this species, Yu et al. (2003) found that
the nicotinic acetylcholine receptors (nAChRs) play a crucial role in acetylcholinesterase from a field strain taken from Florida corn fields
learning and memory due to their participation in fast was up to 85-fold less responsive to inhibition by CBs and Ops
neurotransmission (Taillebois and Thany, 2022). Resistance to (Hilliou et al., 2021).
imidacloprid has been widely investigated in B. tabaci, Aphis The CarE activity reported by various studies, such as alpha and
gossypii, and M. persicae, due to modifications in and subunit of beta esterase production, when exposed to fipronil, was greater in a
nAChR (Xu et al., 2022; Zhou et al., 2022). Synthetic insecticides like resistant strain of the mosquito (Culex quinquefasciatus) than in a
neonicotinoids and spinosad aim to target nAChRs because of their susceptible strain (Sarkar et al., 2009). Increased activity of CarE was
essential role in insect neurotransmission (Kaleem Ullah et al., 2022). detected in beta-cypermethrin-resistant M. domestica when compared
d) The GABA receptor is primarily a Cl—channel, and GABA receptor to beta-cypermethrin-susceptible ones (Zhang et al., 2007). Moreover,
molecules are essential to target locations for multiple chemically elevated esterases activity was reported after insecticides exposure to
diverse kinds of pesticide-active chemicals, resulting in fipronil, the peach potato aphid (M. persicae) (Bass and Field, 2011;
cyclodienes, and avermectins resistance (Burman et al., 2022; Venkatesan et al., 2022) and the brown planthopper (Nilaparvata
Venkatesan et al., 2022). lugens) (Tang et al., 2022). This means that elevated esterases can
detoxify the insecticides. Gene amplification is the cause of the
2.1.5 Metabolic resistance increased production of these enzymes (Şengül Demirak and
Metabolic resistance is a type of resistance inferred by metabolic Canpolat, 2022). In mosquitoes, amplified esterase molecules are
activities in insects that help them detoxify or break down more reactive with insecticides than non-amplified esterases (Gan
contaminants or the ability to eliminate toxic compounds from et al., 2021).
their bodies more quickly (Venkatesan et al., 2022). Insect Insecticide detoxification by CarE has also been reported in other
metabolism is critical in the development of pesticide resistance insect species. For example, some previous studies have indicated an
against various groups of chemical pesticides, including carbamates, increase in the activity of CarE in honeybees following exposure to
organophosphates, and synthetic pyrethroids. Insects metabolize fipronil (Carvalho et al., 2013; Roat et al., 2017). Similarly, the
insecticides to less toxic or non-toxic forms via a mechanism called grassland locust, Epacromius coerulipes Ivanov (Orthoptera:

Acrididae), showed a significantly higher CarE activity in a strain that clade (Nelson, 2011; Zhang et al., 2018). Numerous insect cytochrome
had evolved resistance against fipronil than in a susceptible strain (Jin P450s (CYPs) have been split into eleven families (Hafeez et al.,
et al., 2020). Insecticide metabolism studies indicated that esterases are 2022b). Numerous insect CYPs make up the CYP3 clan of
involved in resistance mechanisms. Increased accumulation of esterase cytochrome P450s, which is further divided into numerous
hydrolytic products in insecticide-resistant insects compared to CYP9 family members known to take part in detoxifying processes
susceptible gives evidence for the involvement of these enzymes linked to pesticide resistance (Schuler, 2011; Hafeez et al., 2019).
(Jensen, 2000; Silva et al., 2012; Khan et al., 2021b; Siddiqui et al., P450 enzymes play an important part in the phase I process of
2022b). detoxification of many different types of hazardous chemicals,
including insecticides, due to their genetic diversity, broad substrate
2.1.5.2 Glutathione S-transferases (GST) specialization, and catalytic adaptability (Kim et al., 2022). For
Glutathione transferases (GSTs) are a broad and diversified herbivorous insects, the main mechanism of pesticide resistance is
family of enzymes that are present in almost all organisms. GST the overexpression of cytochrome P450 detoxifying enzymes (Hafeez
is a class of multifunctional proteins that are extremely important in et al., 2020b; Wu et al., 2021).
the biological transformation of exogenous compounds, drug Different P450 enzymes serve different purposes in insects, such as
metabolism, and protection from peroxidation (Hollman et al., hormone synthesis and regulation, growth and development control,
2016; Dasari et al., 2018). It was discovered that the house fly M. or the digestion of xenobiotic substances (Zhou et al., 2010; Nelson
domestica contains DDT-dehydrochlorinase as a glutathione et al., 2013). Due to their central function in pesticide metabolism,
S-transferase (Clark, 1989). They are crucial for the detoxification cytochrome P450s are frequently implicated in the development of
of both internal and external substances, intracellular movement, the insect resistance to these chemicals (Guo et al., 2012; Panini et al.,
generation of hormones, and the prevention of oxidative stress 2016). One of the most prevalent processes by which insect pests
(Hassan et al., 2019). GST is one of the foremost detoxifying develop resistance to synthetic insecticides is the upregulation of
enzymes of insecticides in insects. Insecticides can be metabolized certain detoxifying P450 enzymes within the insect (Nelson, 2011;
either by reductive dehydrochlorination, which is facilitated by Hafeez et al., 2022a; Luo et al., 2022). Because of this, insecticide
GSTs, or by conjugation reactions with reduced glutathione, resistance may develop as a result of changes in the activity of
which result in water-soluble metabolites that are more easily detoxifying enzymes in insects in response to exposure to
eliminated. Additionally, they help to remove dangerous oxygen- pesticides. Many insect orders, including Coleoptera, Diptera,
free radical species that are formed as a result of the use of Hemiptera, Hymenoptera, and Lepidoptera, have shown evidence
insecticides (Panini et al., 2016). Neonicotinoid resistance in the of P450 overexpression leading to increased resistance to pesticides
B. tabaci is correlated with constitutive overexpression of several (Bass et al., 2011; Johnson et al., 2012; Liang et al., 2015; Wang et al.,
ESTs, GSTs, UGTs, CYPs, and ABC transporters (Vassiliou et al., 2015; Chen et al., 2017; Khan et al., 2021a; Khan et al., 2021c; Hafeez
2011) (Figure 2). et al., 2022a; Siddiqui et al., 2022b).
Several major insecticide types, such as boric acid, carbamates, Invasive species, including B. tabaci, S. exigua, S. invicta, P. xylostella,
organophosphorus, organochlorine, and pyrethrin-resistant in etc., have been demonstrated to exhibit extremely high levels of resistance
German cockroaches, have increased their GST expression levels to to several kinds of insecticides, and this resistance has been linked to CYP
varying degrees (Gentz and Grace, 2006; Nasirian, 2010; Rinkevich detoxifying enzymes (Lai and Su, 2011; Yu et al., 2015; Chen and Zhou,
et al., 2013). Studies on invasive fire ants show that exposure to 2017; Ahmad et al., 2018; Wang et al., 2018b; Xie et al., 2018; Hafeez et al.,
indoxacarb, beta-cypermethrin, and fipronil causes a substantial 2019; 2020a; 2020b; 2022c; Siddiqui et al., 2022b). Increased
alteration in GST activity. Additionally, the outcomes demonstrate transcriptional levels of CYP6AE97, CYP321A9, CYP9A105,
that population resistance and sublethal concentrations substantially CYP321A16, and CYP459 in the midgut of S. exigua larvae treated
impact enzyme activity (Siddiqui et al., 2022c; Siddiqui et al., 2022b). with different insecticides are just some examples of how S. exigua has
OP and DDT resistance mechanisms were reported in houseflies developed a high level of resistance against several types of insecticides
(Ranganathan et al., 2022). In a resistant strain of M. domestica, (Wang et al., 2018a; Hu et al., 2019). Moreover, the detoxification
Zhang et al. (2007) discovered that GST activity was also markedly mechanism by P450 was reported in various studies. For instance, in
elevated. According to Sarkar et al. (2009), the GST activity of all S. invicta belonging to the order Hymenoptera, CYP was involved in the
populations tested was greater than that of a susceptible laboratory detoxification of fluralaner (Xiong et al., 2022) (Xiong et al., 2022), fipronil
strain. Studying orthopterans, researchers found that a particular and beta cypermethrin (Siddiqui et al., 2022b). Similarly, in the order
strain of E. coerulipes had much higher GST activity than Diptera, D. melanogaster, C. quinquefasciatus and Anopheles funestus
susceptible insects (Jin et al., 2020). Insecticide treatments for (Giles) (Daborn et al., 2002; Wondji et al., 2009; Itokawa et al., 2010), in
maize rootworms have already been linked to an increase in GST the order Hemiptera, M. persicae were all reported for the amplification of
activity, according to a recent study (Souza et al., 2020). Pest resistance P450 and insecticide resistance (Puinean et al., 2010). The lambda-
has already been reported in different insects against DDT and OP. cyhalothrin detoxification studies reported the overexpression of
P450 in H. zae and H. armigera (order Lepidoptera) (Li et al., 2000a;
2.1.5.3 Cytochrome P450 monooxygenases (CYP or 2000b; Chen et al., 2017; Hafeez et al., 2020b). Based on these results, it
cytochrome P450) appears that invasive insects rely heavily on the overexpression of
An essential supergene family, cytochrome P450 (P450 or CYP), is P450 genes in order to detoxify xenobiotics from their bodies.
responsible for the metabolism or attenuation of toxicity of numerous
potentially harmful substances (Zhu et al., 2017; Hafeez et al., 2022b) 2.1.5.4 Microbial resistance
(Figure 2). There are four clades in insects where the CYP gene can be Insects host a diverse microbial population that responds to
placed, including CYP2, CYP3, CYP4, and the mitochondrial CYP environmental stresses in a dynamic way (Zhang J. et al., 2022).

Similar to the insect, the associated microbiota are shaped by the armyworm (Spodoptera exempta) have been shown to increase
process of natural selection. Changes in food scarcity and diet resistance to nucleopolyhedrovirus, while the polydnavirus from
chemical exposure can all affect its makeup (Adair and Douglas, parasitoid wasps can disrupt the host insect’s immune system to
2017; Akami et al., 2022). Host microbiota may help the host make sure the survivability of wasp progeny (Strand and Burke,
metabolise pesticides if the host is subjected to selection pressure 2013; Xu et al., 2020). Lower termites, which feed primarily on
from these chemicals. It is possible that this mutation is what makes wood, require symbiotic flagellates to break down lignocelluloses
the host less vulnerable to pesticides (Akami et al., 2019a; 2019b). and methanogenic archaea to produce methane (Ohkuma, 2008;
Bacteria capable of breaking down pesticides have been found in Shi et al., 2015).
numerous natural environments and in several insect orders, Insect microorganisms can modulate insect resistance to synthetic
including Coleoptera (Akami et al., 2019b), Hemiptera (Kikuchi insecticides through direct breakdown and by stimulating the host’s
et al., 2012), Diptera (Cheng et al., 2017; Hassan et al., 2020), and detoxifying enzymes or immune system (Liu and Guo, 2019; Zhao
Lepidoptera (Ramya et al., 2016; Almeida et al., 2017). There has been et al., 2022). For example, the 16S rRNA gene sequencing data
evidence that resistant strains of bacteria from the gut of P. xylostella demonstrated a decrease in the number of the genera Enterococcus
(Xia et al., 2018) and S. frugiperda (Almeida et al., 2017) can break and Stenotrophomonas following polymyxin B therapy, which
down many pesticides (Gomes et al., 2020). Strains of S. frugiperda affected the survival rate of Bombyx mori subjected to chlorpyrifos.
were chosen because of their ability to degrade pesticides; however, The host tolerance to chlorpyrifos was improved when germ-free
these bacteria were lacking in the microbiota of susceptible, unselected silkworms were given S. maltophilia. This bacteria increases host
larvae (Almeida et al., 2017) (Figure 2). acetylcholinesterase activity but cannot directly break down
Insects have a complex defense system built into their digestive chlorpyrifos in the stomach (Du et al., 2020). Aeromonas
tracts, and this system is most likely the driving force behind the hydrophila, an intestine bacteria, was found in substantially greater
organization of gut microbiota (Siddiqui et al., 2022a). Various abundance in deltamethrin-resistant individuals of Culex pipiens.
processes in this defense system influence the host’s tolerance and After antibiotics were used to clear the stomach of the resistant
resistance to bacteria in the insect gut. Though tolerance refers to the strains, the resistance level dropped by 66%, and the host’s
capacity to mitigate the detrimental effects of a particular bacterial cytochrome P450 monooxygenase (CYP450) enzyme function
burden on the host’s health, resistance refers to the capability to lower dropped by 58%. The resistance and CYP450 enzyme activities
the bacterial burden to the point where it is no longer a threat to the were recovered when A. hydrophila was supplied, suggesting that
host’s vigor (Schneider and Ayres, 2008). Insects harboring more A. hydrophila promotes host resistance to deltamethrin by boosting
bacteria in their digestive systems are more tolerant to other foreign CYP450 activity (Xing et al., 2021). Further, P. xylostella intestinal
microbes and have less resistance to them than those with less diverse Enterococcus sp. Upregulates the appearance of an antimicrobial
bacterial communities. Because of this, the systems governing gut peptide called gloverin, which contributes to the insect’s resistance
immunity in various insects might be personalized to the host’s to the pesticide chlorpyrifos (Xia et al., 2018). Wolbachia proliferated
individual needs. Little is known about the systems that mediate in N. lugens after treatment with imidacloprid, and their removal
tolerance, despite the fact that resistance mechanisms have been decreased CYP450 enzyme activities and NlCYP4CE1 transcript
the primary focus of immunology studies (Figure 2) (Engel and levels. This finding supported the hypothesis that Wolbachia
Moran, 2013). However, digestive tract microbe-host interactions increases host resistance to imidacloprid by increasing the
are frequently mutualistic or commensalism in nature. These may expression of the gene encoding the enzyme responsible for its
be of special importance to the host in terms of minimizing any metabolism, NlCYP4CE1 (Cai et al., 2021). The gut microbiome of
harmful effects of the resident microbiota on the host. pollinators like the honeybee (Apis mellifera) increases tolerance to
The insects have a symbiotic microbiome in their guts that aids pesticides like thiacloprid, tau-fluvalinate, and flumethrin by
detoxification (Jing et al., 2020). The enzymatic detoxification method, promoting the expression of genes involved in immunity and
used by invading insects and the intestinal microbiota responsible for detoxification (Wu et al., 2020; Yu et al., 2021). When creating
secreting such digestive enzymes, may be used to establish a viable novel pest control methods or reducing pests’ vector competence, it
resistance development strategy (Figure 2). Developing resistance in a is important to keep an eye on the role of the pests’ microbial partners.
collection of organisms at the same time is undoubtedly difficult (Barbosa Bioremediation and the reduction of xenobiotic toxicity may be greatly
and Levy, 2000). Mutualistic symbiosis plays a significant role in this aided by the discovery of insect-associated microorganisms capable of
process because of its synergy and combined powers; the mutualistic detoxifying hazardous chemicals (Mahapatro, 2017).
alliance formed by two or more species adjusts to adverse conditions (such
as pesticide exposure) more quickly than the individual partners of the 2.1.6 Resistance-inducing operational factors
mutualistic partnership do (Nobre and Aanen, 2012). Accordingly, any The resistance arises from operational factors, including the
beneficial directional flow of resistance development in the system is increased frequency of pesticide applications, the intensive use of
mitigated or reversed by this adaptability. insecticides with increased dosage, decreased yields because of pests,
The generation turnover of symbiotic microorganisms may and environmental damages (Georghiou and Taylor, 1986). In
overcome the barrier of invasive ants’ extended generation time, addition, these factors include a low economic threshold, the
allowing for more favorable mutations or gene regulation/ repetition of the same insecticide use across multiple generations,
alteration, which could lead to pesticide resistance development. the treatment of a large geographical area, the absence of a place of
Few studies on invasive ants have provided evidence of the ants’ refuge, the use of long-lasting, slow-release formulations of the same
ability to metabolize xenobiotic compounds such as lignin, plant allele insecticide, and the use of insecticides that are chemically similar to
chemicals, and pesticides (Engel and Moran, 2013; Siddiqui et al., those previously used (Sarwar and Salman, 2015; Subramanyam and
2022b; c). Three partiti-like viruses isolated from the African Hagstrum, 2018).

3 Challenges in control of invasive where an invasive species is most likely to cause damage, are
species described, emphasizing the environmental factors that must be
present for a pest to establish. However, methods for creating these
Increased global commerce and tourism, climate change, evaluations that are credible, expandable, and cost-effective are
difficulties in protecting borders, Internet commerce, as well as required.
other ways, and invading insects are among global concerns that Particularly in machine learning and other statistical models, the
impose a high economic cost with no apparent remedies in sight difficulty in creating models that can be successfully transferred to new
(Mooney and Hofgaard, 1999; Lester and Keall, 2005; Venette et al., space and time is becoming more widely acknowledged as a
2021). conceptual barrier (Morey and Venette, 2020). While process-based
Managing invasive species is challenging because they are often models appear promising, the sheer volume of information needed to
hard to find, and the damage they do may not be noticed for a while. apply them to the hundreds or even thousands of species of
Another challenge is developing new strategies to detect or manage importance makes them impractical (Venette, 2017). Improvements
invasive species. Frequently traditional management practices are in the ability to record shifts in insect population abundance,
being used to manage new species, but our ability to control a new distribution, and phenology directly result from the
invasive species often requires developing novel tools. The last democratization of data collecting made possible by the rise of
challenge is funding for invasive species control, where there is less mobile apps and open-access databases. To strengthen predictions,
support for interdiction activities and extremely high expenditures advances in phylogeography will allow for a more thorough
to launch large-scale actions against established species. Most accounting of invasions, the identification of invasive phenotypes,
efforts to control and study invasive species fall into two phases. and the explicit consideration of genotype x environment
The initial phases of an invasion (forecast and prevention) give way relationships (Estoup and Guillemaud, 2010; Roe et al., 2019).
to later phases (early detection, fast response, mitigation, and Early detection surveys can be more efficiently planned with the
management) as the invasion moves forward through the help of pest risk maps, which identify probable invasion or damage
arrival, settlement, and spreading phases (Venette et al., 2021). regions. Our current capacity for surveying the endangered area may
Cost-benefit evaluations show that focusing on prevention and be inadequate (Venette et al., 2010). More study is required, in our
containment rather than damage control and ecosystem opinion, to determine the likelihood of finding low concentrations of
restoration is the best way to deal with invasive species (Leung invasive arthropods using a given sample strategy (Sandercock et al.,
et al., 2002; Lampert and Liebhold, 2021). Sociologists term the 2022). Experts devised a “risk-based monitoring” method that
spread of alien invasive species a “wicked” problem because of the concentrates its sampling efforts in areas with the greatest density
complex interplay between its many root causes (such as of the invasive pest preferred and most economically valuable host
globalization, climate change, public ignorance, and inadequate plants (Prattley, 2009). As a result, we can lower the expense of
biosecurity measures) (McNeely, 2013; Venette and Morey, 2020). detecting invasive species, while additional studies are needed to
Researchers may do their part to control invasive species by determine whether or not this method is effective for invading
focusing on objectives that have widespread support and can be insects. It can be computationally challenging to utilize the
measured quantitatively. The costs and advantages of a proposed strategies pioneered by Yemshanov et al. (2017, Yemshanov et al.
solution (such as a new sample plan or control system) should be 2019) to optimize the spatial distribution of sampling efforts.
clearly stated and compared to the status quo. Multiple reasons When combined with conventional taxonomical knowledge, the
have led to an increase in the number of invasive species that have recent advancements in genomes provide a method for quick
migrated over political and natural boundaries, necessitating a validation of species identification. Additionally, genomic
multifaceted approach to eradicating them. techniques allow for the differentiation of strains, haplotypes, or
biotypes within a species (Venette et al., 2021). To better depict the
geographic origins of an invading population, specific haplotype data
4 Management strategies can be used, as shown for the S. frugiperda (Goergen et al., 2016), H.
halys (Xu et al., 2014), and walnut twig beetle (Pityophthorus
The best strategy for combating exotic species is based on juglandis) (Rugman-Jones et al., 2015). Precise pest origin
prediction and prevention. The goal is straightforward: predict information allows for early country selection in the search for
which species or pathways provide unacceptable dangers and natural enemies, typically species-specific parasitoids, which may
prevent them from entering a target area. Such a plan necessitates then be released in invaded nations after being evaluated for safety
a defined indicator of success. As the number of alien arthropods keeps and efficacy (Wyckhuys et al., 2020; Venette et al., 2021).
rising, every new invasion could be seen as a breach in biosecurity Following the initial settlement and expansion of invasive species,
(Finch et al., 2021). However, international trade has expanded faster it is prudent to invest immediately in R&D to promote integrated pest
than new species have been introduced. This pattern implies management (IPM) strategies. IPM is “an ecosystem-based strategy
biosecurity measures have been relatively effective (Venette and that focuses on long-term prevention of pests or their damage through
Morey, 2020) but are distant from an accurate degree of success a combination of techniques such as biological control, habitat
(Saccaggi et al., 2016). manipulation, modification of cultural practices, and use of
To determine whether or not a product can be legally imported, resistant varieties (Sujatha et al., 2022). Pesticides are used only
how surveillance programs should be set up, and what actions should after monitoring indicates they are needed according to established
be taken after an invasive species has been discovered in a sensitive guidelines, and treatments are made to remove only the target
area, biosecurity professionals will continue to rely on spatially- organism (Singh et al., 2018). Pest control materials are selected
explicit pest risk assessments (Venette et al., 2010). Locations and applied to minimize risks to human health, beneficial and

non-target organisms, and the environment” (IPM, 1996). These affect the nation’s economy. Scientists must work together across areas
decision-making guidelines are applied to pest management on a in order to detect invasive pests and analyze their ecological problems,
regional scale rather than just on a farm or a piece of land. Ironically, environmental risks in different habitats, financial damage, and
many cropping systems already have IPM in place for indigenous management alternatives. This can be done by creating generic,
pests. In the case of H. halys in the U.S. apple crop, for particular, and context-dependent action plans. This highlights the
example, >$37 million was wasted related to destruction and significance of the quarantine in preventing the spread of destructive
elevated insecticide application costs because of the advent of the alien pests.
pest (Leskey and Nielsen, 2018). IPM solutions for invasive species
often involve short- and long-term plans, just as they do when dealing
with endemic pests. Pesticidal treatment is frequently prioritized first Author contributions
since it is effective at maintaining growers’ capital, although
agreements to fund research into biocontrol, pest-resistant The initial draft was written by JS, RF, HN, and BB. The
cultivars, and cultural measures (Radcliffe et al., 2009), physical manuscript was supervised and financially supported by XC and
exclusions (Rogers et al., 2016), and “attract and kill” behavior- YW. The document was conceptualized and developed by JS, YX
based insect traps (Gregg et al., 2018). Developing resistance to and XC. MH, MG and YW provided critical feedback and reviewed the
invasive pests is becoming increasingly crucial for trees and paper. BB, MH and YX revised the manuscript. All authors have read
perennial crops. Innovative technologies, such as transgenic and agreed to the final version of the manuscript.
insecticidal plants or genetic biocontrol agents facilitated by gene
drives, have the potential to either complement or replace IPM
programs, depending on whether or not they are granted the Funding
necessary regulatory permissions (Hutchison et al., 2010) (Maselko
et al., 2017; Sudweeks et al., 2019). This study was supported by the National Key Research and
Development Program of China (2021YFE0107700), Science and
Technology Base and Talent Project of Guangxi Province (Guike
5 Future implications AA21196003), Guizhou Provincial Science and Technology
Program (2019-1410; 2021-229; HZJD[2022]001), Outstanding
Insect invasions caused by globalization have posed a severe Young Scientist Program of Guizhou Province (KY2021-026),
danger to native plant and animal life, with some species becoming Guangxi Key Laboratory of Rice Genetics and Breeding Opening
extinct. Because of increased international trade, more seeds and Research Project (2022-36-Z01-KF12), Guizhou University
other planting materials are being transported worldwide, Cultivation Project (2019-04), Program for Introducing Talents
increasing the risk of invasive pests being introduced into new to Chinese Universities (111 Program; D20023), and Program for
habitats and countries. Introducing Talents to Chinese Universities (111 Program;
As a matter of biosecurity, it is recommended that invasive species D20023).
be identified as soon as possible to control them from invading new
regions. However, many underdeveloped nations are particularly
lagging in early detection. Without natural predators and parasites, Conflict of interest
invasive species in their new environment can quickly spread and
cause severe damage to economically important plant species and The authors declare that the research was conducted in the
biodiversity. absence of any commercial or financial relationships that could be
Strategies to prevent or lessen the impact of future incursions construed as a potential conflict of interest.
should be part of any future approach to managing invasive species. It
is possible to reduce the likelihood of introducing new pest species into
an area if people have a general knowledge of invasive species and Publisher’s note
work together globally by sharing data about these organisms and the
predators and parasites that threaten them. The increased science- All claims expressed in this article are solely those of the
based knowledge, innovation, and expertise in managing invasive authors and do not necessarily represent those of their affiliated
species helped control them more efficiently. organizations, or those of the publisher, the editors and the
The local flora and fauna, agriculture, horticulture, and the reviewers. Any product that may be evaluated in this article, or
environment severely impact the harmful impacts of invasive pest claim that may be made by its manufacturer, is not guaranteed or
species. These species negatively impact biodiversity and may also endorsed by the publisher.
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Insights Into Insecticide-Resistance Mechanisms in Invasive Species

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TYPE Review

PUBLISHED 09 January 2023

Insights into insecticide-resistance

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biological invasion, insecticide resistance, biodiversity risk, exotic species, resistance

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TABLE 1 A list of insecticide-resistant invasive species of China.

Scientiﬁc name Common Resistance against insecticide Country References

Bactrocera cucurbitae Dacus cucurbitae Organophosphorus; pyrethroid China Gu et al. (2015)

Cydia pomonella Codling moth Chlorpyrifos; carbaryl China

Lissorhoptrus Rice water weevil Chlorphenamide China Liu et al. (2018)

Pectinophora Pink bollworm Decamethrin China Li et al. (1995)

Periplaneta American cockroach Neonicotinoid China Zhang et al. (2018)

Spodoptera fall armyworm Indoxacarb China Hafeez et al. (2021, 2022a)

Trogoderma khapra beetle Phosphine China Borah et al. (1981)

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TABLE 2 A list of insecticide-resistant invasive species in the world.

Scientiﬁc name Common Resistance against Country References

Imidacloprid Europe Wang et al. (2011)

Glutathion; Chlopyrifos; Phosalone Spanish Rodríguez et al. (2010)

Periplaneta Americana Imidacloprid America Wang et al., 2004,2006; Ko et al., 2016

Periplaneta Australian Abamectin America Wang et al., 2004,2006; Ko et al., 2016

TABLE 3 Insecticide classiﬁcation based on target site.

Chemical group Insecticide Target site

Pyrethroids alpha-cypermethrin, deltamethrin, and permethrin Sodium channel modulators (Nav)

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