INTRODUCTION
Pesticide resistance development brings immense challenges for global agriculture and is a
prime example of rapid evolution induced by human activities (Chen & Schoville, 2018;
Rosenheim et al., 1996).
Such resistance has been defined as a ‘genetically based decrease in susceptibility of a
population to a toxin caused by exposure of this population to the toxin in the field’
(Tabashnik et al., 2013).
It often follows soon after a new synthetic compound is introduced (Palumbi, 2001) due to
the strong directional selection that pesticide application exerts on pests. It was, however,
recently highlighted that the evolutionary history of a species might affect the likelihood of
developing resistance, making some species more predisposed to evolve resistance than
others (Dermauw et al., 2018; Hardy et al., 2018; Walsh et al., 2022).
In this context, phytophagous arthropods have been suggested to be pre-adapted to handle
chemical insecticides since they have evolved to tolerate and resist their host
plant's allelochemicals (Rosenheim et al., 1996; Després et al., 2007; Box 2).
As a general extension, we can thus define cross-resistance as resulting from prior exposure
to a different, possibly not chemically related, toxin in a species' evolutionary history. The
evolution of cross-resistance is expected to be more prominent in generalist arthropod
species (Dermauw et al., 2018; Hardy et al., 2018) since they have to detoxify or metabolise
a broader range of plant defensive chemicals than specialist species (Cheng et al., 2017;
Box 3).
The influence of plant–arthropod evolutionary interactions on pesticide resistance
development has furthermore been shown as insects feeding on herbaceous plants are more
likely to evolve pesticide resistance than insects feeding on other plant groups (Hardy et
al., 2018). Although this pattern may be confounded by the amount of pesticide use
(Dermauw et al., 2018), correction for this factor still implies that certain insect groups are
more likely to develop pesticide resistance (Crossley et al., 2021; Hardy et al., 2018).
Moreover, experimental evidence suggests that pesticide resistance can evolve when
arthropods expand their host plant range. For example in the two-spotted spider mite,
when a susceptible strain adapted to a novel host, the detoxification gene expressions
resembled those of multi-insecticide-resistant populations (Dermauw et al., 2013).
Allelochemical: A chemical produced by an organism that is toxic to, inhibits the growth or
affect the physiology, behaviour or life history of, other organisms; synonymous here with
‘plant defensive chemical’ (adapted from Després et al., 2007).
Cross-resistance: The ability to tolerate and resist chemical toxins from a new source
following adaptation to chemical toxins from another source, for example cross-resistance
to pesticides following adaptation to a new host plant.
Resistance to pesticide treatments was first noted over 100 years ago (Melander, 1914), and
since then, an increasing number of insects have evolved resistance to at least one or more
of the available insecticides (Feyereisen et al., 2015; Taylor et al., 1983). As in other cases of
resistance evolution, pesticide resistance develops following strong directional selection on
the pest. Arthropods have developed several different mechanisms, from behavioural to
molecular, to withstand pesticides (Figure 1) that are similar to the strategies that
arthropods have evolved in response to chemical host plant defences (e.g. behaviour or
detoxification) (Després et al., 2007; Heckel, 2014).
IGURE: Number of publications found on primary research on web of science investigating
the proportion of studies on pesticide resistance with an ecology, evolution or genetic
approach from 1985 to 2021.
Ecological conditions that may facilitate
Pesticide resistance evolution
Ecological research has provided numerous examples of host plant shifts or expansions in
arthropods, in some cases due to geographical range changes (Audusseau et al., 2017;
Battisti et al., 2005; Diegisser et al., 2009; Sánchez-Guillén et al., 2016; Singer &
Parmesan, 2021).
In light of this gathered knowledge, we develop below different contexts where arthropods
may be exposed to new host plant species, and pesticide resistance may evolve as a
consequence through cross-resistance.
During geographical range expansion, a phytophagous species may encounter novel plant
species, which could lead to a modification of its diet breadth (i.e. Hill et al., 2011; Jahner et
al., 2011; Lancaster, 2020) where the ability to change or increase its host plant range could
favour the species establishment by exploiting new resources (Battisti et al., 2005).
Under natural or climate-driven expansion, the expanding arthropod population may
encounter a gradual shift in the plant community. On the contrary, part of the arthropod
population is transported via human activities outside their native range during invasion
(Blackburn et al., 2011). In this case, the introduced individuals may have to face entirely
novel host plant communities and need to adapt to those communities in order to persist in
the new environment (Hill et al., 2016).
Therefore, selection for adapting to new host plant species may be more assertive in
invading species than in species naturally expanding their range (Renault et al., 2018).
Hypothetically, cross-resistance to pesticides would thus be more often found in invading
species if they have been repeatedly selected to adapt to new host plant communities.
Ecological consequence of Pesticide
resistance development
The insight that pesticide resistance may evolve as cross-resistance through new or
improved abilities to tolerate and resist plant allelochemicals, opens up the possibility that
pesticide resistance development, in turn, may facilitate an expansion of arthropods' host
plant range, that is a converse cross-resistance scenario. Since also non-target species may
be exposed to enough insecticides to evolve resistance mechanisms (e.g. Rdl dieldrin
resistance in Drosophila melanogaster, ffrench-Constant et al. 2000), converse cross-
resistance may thus have significant ecological consequences for
the agroecosystems through altered host plant ranges in both pests and non-target species
(Figure 3). Adaptation to a novel host plant may affect various biological traits (Box 3),
making the evolutionary outcome unpredictable (Fox et al., 2017). Such trait evolution may
further lead to both direct and indirect eco-evolutionary effects up to the species
community scale (Utsumi, 2011).
FIGURE: Scheme over pesticides' direct and indirect impacts on ecosystem functioning
following cross-resistance, from target species to non-target species. Pesticides, the
development of resistance due to their use
Besides the notion that arthropods' adaptation to novel host plants may lead to pest
problems on their new hosts, an increased host plant range in pest arthropods could
enhance the ability to persist in unexplored areas and thus facilitate geographical range
expansion. For pest arthropods, utilizing additional hosts may further disrupt control
strategies as pests could persist using alternative host plants as refuges (Montezano et
al., 2018; Figure 3).
Cross resistance: Taking ecology in to
account
However, adopting a novel host plant comprises arthropods' ability to feed, but also locate
and accept the host plant through oviposition (Harvey et al., 2010).
Cross-resistance may thus likely increase arthropod performance on new host plants
through the ability to withstand and detoxify the allelochemicals, but whether preference
for the new host plant species also could be affected or not needs to be assessed.
Perhaps cross-resistance enhances performance on novel hosts in the first step, while
preference evolves later. However, in cases where females prefer a plant species on which
larvae perform poorly, cross-resistance that allows her offspring to have a better feeding
performance on this plant may allow both the preference and performance of this host
plant to spread rapidly in the population. This may be a more likely scenario in generalist
species, where mothers' preference and offspring performance are not always correlated
(Gripenberg et al., 2010).
If pesticide resistance development could lead to host plant range changes through cross-
resistance, this may have consequences for general food-web and community dynamics
involving non-target species. For example host shifts may affect herbivore competition on
the novel host plant (Carrasco et al., 2018), and the evolution of new feeding traits may
impact the arthropod community through indirect eco-evolutionary effects mediated
between the shared host plant (Utsumi, 2015).
Furthermore, we predict that adopting novel host plants through cross-resistance could
involve acquired mechanisms to tolerate new classes of allelochemicals which could affect
higher trophic levels' preference and performance.
If a phytophagous species uses those new allelochemicals to defend against parasitoids and
predators (compare Harvey et al., 2010; Bezemer et al., 2014), through sequestration
(Beran & Petschenka, 2022), the efficiency of its natural enemies may be affected.
This could have suppressed or released effects on the herbivore, depending on whether the
higher trophic levels have advantages or disadvantages from the novel host traits (compare
Harvey et al., 2010; Grosman et al., 2017), and may lead to further evolutionary responses
between the host and the natural enemy. Moreover, an altered host plant range in
herbivorous pollinators such as within Lepidoptera may affect plant–insect mutualisms
and their ecosystem service capacity. It has previously been argued that a multitrophic
perspective should be taken on novel host plant–insect associations to fully understand
their consequences (Harvey et al., 2010), and this may therefore be relevant also for cross-
resistance following pesticide resistance development.
An altered host plant range following pesticide resistance development may thus have
consequences, for example on trait evolution, competition, niche occupation, trophic
interactions and range expansion, which may impact community dynamics in the entire
agroecosystem. To understand these dynamics, it may also be relevant to take into account
that resistance development itself may come at a cost (Carrière et al., 1994; Gutiérrez et
al., 2019), affecting reproduction (Abbas et al., 2012), population dynamics (Boivin et
al., 2003) or species interactions (Bendis & Relyea 2016). However, very little is known
about the community-scale consequences of pesticide resistance development, and we may
thus only have understood a minor part of the effects of pesticide application on species
inhabiting the agroecosystem. In this context, it would be useful to take an eco-evolutionary
perspective to address plausible feedback loops between trait evolution and community
ecology following cross-resistance. Further empirical studies in the lab and the field
combined with theoretical modelling are thus warranted to better understand the
ecological and evolutionary consequences of pesticide resistance development in
arthropods. Such studies will be beneficial from a pesticide resistance management
perspective and gather knowledge on eco-evolutionary dynamics in natura (Hendry, 2019).
Cross resistance: Taking ecology in to
account
More profound knowledge about the emerging field of arthropod gut microbiota could
provide novel insights on its role in mimicking cross-resistance between pesticides and
defensive plant chemicals (Box 2).
Herbivorous arthropods Harbor gut microbiota that has been suggested to aid in plant
allelochemical detoxification (Ceja-Navarro et al., 2015; Després et al., 2007; Francoeur et
al., 2020) even if its importance may vary between insect orders (Hammer et al., 2017).
Interestingly, other pesticides, such as herbicides and fungicides, may also select for
adaptation in arthropods (Dubey et al., 2020; Rainio et al., 2019).
Exposure to multiple pesticides may, at worst, select for pests that become multi-resistant
to a wide array of toxins. If there is cross-resistance in both directions, from host plant
adaptation to pesticide resistance and vice versa, would such multi-resistant arthropods
also be able to shift or increase their host plant range to a larger degree? Perhaps, the
additive effects of an increased amount of toxins, both concerning doses and variety of
compounds, in the environment may select a higher ability to increase host plant range in
both pest and non-pest species with ecological consequences. Pesticide resistance and
ecological consequences such as host plant range may thus vary between environments with
high or low toxins levels in time and space.
Taking cross resistance in to Account in pest
management strategies
Increased knowledge about the evolutionary links between pesticide resistance and host
plant adaptation, together with the ecological context and consequences, is of great interest
both from a fundamental research aspect and a pest management perspective.
Indeed, a better understanding of which species and in which circumstances pesticide
resistance evolves would improve resistance monitoring and resistance management.
Pesticide resistance is a common problem across species groups (Sparks & Nauen, 2015),
and preferably resistance monitoring and management should be included in pest control
strategies to avoid further resistance development (Karlsson Green et al., 2020).
For example, reducing pesticide use and developing new control strategies for species that
are more likely to develop resistance will be necessary. This perspective may also be of
interest for breeding programs to avoid consequences on pesticide resistance development
and host plant range from interacting effects between pesticides and plant chemical
defenses.
In sustainable pest management, biopesticides based on naturally occurring organisms or
allelochemicals could be used (Fenibo et al., 2021).
Due to the potential for pre-adaptation and cross-resistance, these substances should be
selected by care to minimise the potential for resistance development and host range
expansion. However, overuse of biopesticides can still lead to resistance, for example
granulovirus in the codling moth (Asser-Kaiser et al., 2007) or Bacillus thuringiensis (Bt) in
the diamondback moth (Tabashnik et al., 1991).
CONCLUSIONS
The widespread use of pesticides in agricultural production has initiated a massive
experiment in microevolution at a global scale (Rosenheim et al., 1996) and has created
ecosystems that can be excellent subjects for evolutionary (Karlsson Green et al., 2020) and
eco-evolutionary studies (Hendry et al., 2017).
However, it also created, at the same time, environments (more) challenging to manage due
to resistance evolution.
More research on links between host plant range and pesticide resistance evolution is
needed to confirm this pattern.
Understanding the ecological and evolutionary consequences of pesticide resistance in
target and non-target arthropods will unravel the potential impact of pesticides on
multitrophic interactions and ecosystem functioning, which could aid in developing more
sustainable pest management strategies.
R E F E R E NC E
Abbas, N., Shad, S.A. & Razaq, M. (2012) Fitness cost, cross re-
sistance and realized heritability of resistance to imidaclo-
prid in Spodoptera litura (lepidoptera: Noctuidae). Pesticide
Biochemistry and Physiology, 103, 181–188.
Acuna, R., Padilla, B.E., Florez-Ramos, C.P., Rubio, J.D., Herrera,
J.C., Benavides, P. et al. (2012) Adaptive horizontal transfer of a
bacterial gene to an invasive insect pest of coffee. Proceedings of
the National Academy of Sciences, 109, 4197– 4202.
Agosta, S.J. & Klemens, J.A. (2008) Ecological fitting by phenotyp-
ically flexible genotypes: implications for species associations,
community assembly and evolution: ecological fitting. Ecology
Letters, 11, 1123–1134.
Ali, J.G. & Agrawal, A.A. (2012) Specialist versus generalist insect her-
bivores and plant defense. Trends in Plant Science, 17, 293–302.
Amarillo-Suárez, A., Repizo, A., Robles, J., Diaz, J. & Bustamante,
S. (2017) Ability of a generalist seed beetle to colonize an exotic
host: effects of host plant origin and oviposition host. Neotropical
Entomology, 46, 368–379.
Amezian, D., Nauen, R. & Le Goff, G. (2021) Transcriptional regula-
tion of xenobiotic detoxification genes in insects - an overview.
Pesticide Biochemistry and Physiology, 174, 104822.
Andersen, E.M., Cambrelin, M.N. & Steidl, R.J. (2019) Responses
of grassland arthropods to an invasion by nonnative grasses.
Biological Invasions, 21, 405– 416.
Anderson, P. & Anton, S. (2014) Experience-based modulation of be-
havioural responses to plant volatiles and other sensory cues in
insect herbivores: experience modulates herbivore behaviour.
Plant, Cell & Environment, 37, 1826–1835.
Asser-Kaiser, S., Fritsch, E., Undorf-Spahn, K., Kienzle, J., Eberle,
K.E., Gund, N.A. et al. (2007) Rapid emergence of baculovirus
resistance in codling moth due to dominant, sex-linked inheri-
tance. Science, 317, 1916–1918.
Audusseau, H., Le Vaillant, M., Janz, N., Nylin, S., Karlsson, B. &
Schmucki, R. (2017) Species range expansion constrains the eco-
logical niches of resident butterflies. Journal of Biogeography,
44, 28–38.
Babendreier, D., Koku Agboyi, L., Beseh, P., Osae, M., Nboyine,J., Ofori, S.E.K. et al.
(2020) The efficacy of alternative,14610248, 2022, 8, Downloaded from
https://onlinelibrary.wiley.com/doi/10.1111/ele.14030 by Jimma University, Wiley Online
Library on [20/06/2023]. See the Terms and Conditions
(https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of
use; OA articles are governed by the applicable Creative Commons License
