Trade-offs between chemical resistance to herbivory and responses to abiotic stresses in invasive plants

INTRODUCTION

Plants change their traits to respond to shifting environments, enabling them to defend against biotic stresses such as herbivorous insects, and/or tolerate abiotic stresses, such as extreme climate (Callaway et al. 2022; Zhang et al. 2018, 2022). There are often costs when plants produce secondary chemicals to adapt to varying biotic or abiotic environments (Abdala-Roberts et al. 2016). Given that plant resources are limited and some of their physiological processes are closely linked, plant chemical responses to abiotic and biotic environments may be related (Nawaz et al. 2023). Therefore, changes in responses to abiotic (or biotic) stresses may affect responses to biotic (or abiotic) stresses, and plants could trade-off their defenses against those environment factors.

Trade-offs between chemical defenses to varying environments may be particularly important for invasive plants (Defossez et al. 2018; Feng et al. 2009). As many invasive plants in their introduced ranges need to adapt to environments that likely differ with from those in their native ranges, they may effectively trade-off their defenses to the changing environmental stresses to improve their performance, eventually leading to their invasion success (Yang et al. 2021; Yuan et al. 2022). In this context, invasive plants may adjust resource allocation to cope with these changing environments. On the one hand, invasive plants often ‘escape’ from co-evolved specialist enemies when introduced from their native ranges into invasive ranges (Joshi and Vrieling 2005). Thus, the invader defensive chemicals and the genes that regulate these chemicals could change accordingly (Bieker et al. 2022; Sun and Roderick 2019). On the other hand, in introduced ranges, invasive plants also need to produce secondary chemicals to tolerate abiotic stresses, such as climate (Xiao et al. 2020a).

Since some chemicals that are both involved in resistance to herbivory and response to abiotic stresses share the same biosynthetic pathways, changes in invasive plant defenses against insects and abiotic stress may be closely related. Therefore, given that there are often decreasing resistances to insects in invasive plants due to the ‘enemy release’, the invasive plant defenses to abiotic stress may be increased, i.e. invaders could trade-off their defenses by adjusting chemical allocations to improve their performance. Furthermore, since some specialist herbivores may be accidently or deliberately introduced into the same ranges where their host plants are invading, leading to reassociation with invasive plants (Wan et al. 2019; Zangerl and Berenbaum 2005). In response to this reassociation, invasive plants may restore their chemical defenses against insects, but at the cost of tolerance to abiotic stress (Yin et al. 2023). Testing these hypotheses could improve our understanding of how chemical defenses evolve to adapt to the changing biotic and abiotic environments in invasive plants.

INVASIVE PLANT RESISTANCE TO HERBIVOROUS INSECTS

Natural enemy and EICA hypothesis

Natural enemy hypothesis is one of the most prominent theories that explains why invasive plants often grow larger than native ones (Keane and Crawley 2002). This theory posits that, during the invasion process, invasive plants escape natural enemies from their native ranges, particularly co-evolved specialists, and thus gain advantages over native plants for their growth and competition with natives (Keane and Crawley 2002). This theory has been supported by numerus reports comparing differences in natural enemies and their damages to plants from introduced and native populations of invasive species. For example, Xiao et al. (2020b) reported greater damage by chewing herbivores, and more abundance of sucking herbivores on plants of the invasive Chinese tallow tree (Triadica sebifera) in its native range than those in its introduced range.

Based on the Natural Enemy Hypothesis, the Evolved Increased Competitive Ability (EICA) hypothesis predicts that, given that invasive plants are no longer under high pressure from natural enemies, such as specialist insects, they reallocate resources by decreasing defenses against insects but increasing resources for plant growth and reproduction (Blossey and Nötzold 1995; Callaway et al. 2022). Many studies have found reduced defenses against specialist insects but increased plant performance in introduced populations compared with native populations. For example, Huang et al. (2010) found that the biomass of the specialist caterpillar Gadirtha inexacta reared on plants of introduced populations of T. sebifera was significantly higher than those on plants of native populations of the same species, while plants of the introduced populations with higher C:N grew bigger than plants of the native populations, suggesting that resource allocation during the plant invasion process results in reduced resistance to specialist insects but improved plant performance.

Chemical responses to changing natural enemies

Secondary metabolites have many important functions for plants, such as defending themselves against herbivores and pathogens, serving as agents mediating plant–environment interactions (Erb and Kliebenstein 2020; Walker et al. 2022). For example, terpenes, produced via the mevalonate or methylerythritol phosphate pathway (Divekar et al. 2022), act as defensive toxins or herbivore deterrents. Phenols are derived from the shikimate pathway; many of them such as flavonoids, lignin and condensed tannins function as defensive chemicals against pests, fungi and other abiotic stresses (Erb and Kliebenstein 2020; Jan et al. 2021).

For invasive plants, escape from specialist herbivores can trigger evolution of chemical defenses. For example, tannins are effective in defending against many specialists, but their concentrations in plants vary depending on the abundance of specialists. Studies found that there were lower concentrations of tannins in plant leaves of the introduced populations of T. sebifera than in the native populations of the invader, due likely to the absence of specialists in introduced ranges of this plant (Wang et al. 2012; Xiao et al. 2020b).

Reassociation with co-evolved specialists and the ‘restored’ chemical resistances

Though invasive plants escape from natural enemies of native ranges and co-evolved specialists are left behind during invasion process, some specialist herbivores may be accidently (e.g. via agricultural products) or deliberately (e.g. classical biological control) introduced to the same ranges where their host plants are invading, leading to reassociation with invasive plants (Müller-Schärer et al. 2014; Zangerl and Berenbaum 2005). Thus, after specialist insects being reassociated with the invasive plant host, the plant chemical resistance could be enhanced again, i.e. invasive plants could restore their chemical defenses under the pressure of the specialists. For instance, when herbarium specimens of the invasive weed, Pastinaca sativa, were examined, Zangerl and Berenbaum (2005) found that the defensive phytochemical furanocoumarins in the plant were declined in the introduced populations, but then increased after accidental introduction of the parsnip webworm, Depressaria pastinacella.

Similarly, Fukano and Yahara (2012) and Wan et al. (2019) found that the invasive plant Ambrosia artemisiifolia L. (Asteraceae) evolved higher defenses against insects after reassociation with the specialist beetle Ophraella communa Lesage (Chrysomelidae: Coleoptera) in non-native ranges. Yin et al. (2023) conducted further studies on the differences of secondary chemicals between populations of A. artemisiifolia with different reassociation histories with the specialist beetle. They found that the concentrations of tannins and lignins were higher in reassociation populations than those in non-reassociation populations, corresponding with the changes in resistance to the insect along the reassociation gradient.

INVASIVE PLANT RESPONSES TO ABIOTIC STRESSES

Invasive plants could enhance their abiotic stress tolerance to UV, drought and salinity to enable them to persist in a novel habitat in their introduced ranges (Lu et al. 2022; Marchini et al. 2019; Yu et al. 2022). For example, the invasive Chromolaena odorata displayed significantly lower energy dissipation than its native conspecific after 2 months of drought treatment, suggesting that the invasive C. odorata may develop a higher degree of drought tolerance than its native conspecifics (Li et al. 2022). This finding is in agreement with the results of Zhang et al. (2023) who also found that invasive plant species might exhibit a greater recovery from drought following rewetting than co-occurring native plant species. Deng et al. (2017) reported that, enhanced UV-B radiation resulted in more resources of the invasive populations of T. sebifera being allocated to the leaves to resist external UV-B radiation stress. With regard to tolerance to soil salinity, previous studies have shown that the invasive T. sebifera seedlings have greater tolerance of salinity, with high survival and biomass compared with native trees, allowing the invader to invade and dominate coastal habitats in its introduced range (Yang et al. 2015, 2022).

Many metabolisms are known to facilitate the response of plants to abiotic stresses (Mathesius 2018; Tattini et al. 2004). For example, the production of proline, soluble proteins, soluble sugars, malondialdehyde, free amino acids and antioxidant enzymes (superoxide dismutase, peroxidase and catalase) can be significantly induced by drought stress in Cenchrus pauciflorus Benth (Zhou et al. 2021). In particular, the antioxidants (e.g. flavonoids and chlorogenic acid) in phenylpropanoids play crucial roles in plant responses to abiotic stress (Dong and Lin 2021; Fuchs et al. 2021). Xiao et al. (2020a) found that the invasive populations of T. sebifera at low latitudes produced relatively more flavonoids to increase tolerance to solar radiation and then promoting growth, suggesting that plants may optimize chemical productions to adapt to changing environments.

CHEMICAL-MEDIATED TRADE-OFFS BETWEEN RESISTANCE TO HERBIVORY AND RESPONSES TO ABIOTIC STRESSES IN INVASIVE PLANTS

Trade-offs between defenses to insects and abiotic stresses

In response to different biotic and/or abiotic stresses, plants allocate resources to the biosynthesis of different secondary metabolites (Mertens et al. 2021; Yin et al. 2023). Given that some secondary metabolites are produced by the same biosynthetic pathways and may share the same precursors (Dong and Lin 2021; Fuchs et al. 2021), the production of these secondary metabolites within the pathways may be negatively correlated. Thus, there are potentially trade-offs between plant responses to different stresses (Berens et al. 2019; Xiao et al. 2020a). If plants produce more chemicals responsible for defending against insects, and these chemicals share the same biosynthetic pathways with another class of chemicals responsible for abiotic stresses such as drought, then, the plants may have low tolerance to drought. For example, many plants produce flavonoids in response to abiotic stresses, such as UV and drought (Mierziak et al. 2014; Zhao et al. 2021), and these plants may also produce tannins and lignins, which share the same biosynthetic pathways with flavonoids (Dong and Lin 2021). In this case, increasing tannins by plants for high resistance to insects may come at the cost of decreasing flavonoids and low tolerance to some abiotic stresses (Xiao et al. 2020a).

Plant invasion and trade-offs between resistance to insects and tolerance to abiotic stresses

Plant invasions provide ideal opportunities to investigate trade-offs between resistance to insects and tolerance to abiotic stresses, given that invasive plants are released from co-evolved specialist insects but also need to cope with abiotic environments in their introduced ranges. As discussed earlier, decreased chemical resistance to specialists is expected in introduced populations of an invasive species, relative to native populations of the same species. If plants could trade-off chemical resistance to insects and tolerance to abiotic stresses, then invasive populations of an invader with low resistance to insects may show high tolerance to abiotic stresses. This may be also expanded to studies that compare the differences of these defenses between invasive plants and their closely related native species, i.e. invaders likely show low resistance to insects but high tolerance to abiotic stresses, relative to their native congeners.

The evolutionary process of trade-offs between resistance to insects and tolerance to abiotic stresses could be reversed by the subsequent introduction of native specialist herbivores. Yin et al. (2023) simultaneously compared resistance to insects and tolerance to droughts in populations of the invasive plant A. artemisiifolia that had different history of reassociation with the specialist beetle, O. communa. They reported that, increasing time since reassociation was correlated with increasing leaf concentrations of the defensive chemicals (e.g. tannins and lignins) but decreasing leaf concentrations of the antioxidant compounds (e.g. flavonoids and chlorogenic acid). Changes in these chemicals indicated that plants reallocated phytochemical resource from investment in abiotic stress tolerance to investment in biotic stress resistance, driven by the co-evolved specialist herbivore. Moreover, they conducted transcriptomic profiling of the plant leaves, showing that these chemical changes were corroborated by shifts in the expression of underlying biosynthetic genes and plant antioxidants. Their work suggests that the specialists could trigger rapid evolutionary trade-offs between abiotic and biotic stress responses in invasive plants.

The study by Yin et al. (2023) is the first to report the evolution of trade-offs between resistance to insects and tolerance to drought in invasive plants. Whether this is also the case for other invasive plants warrants further studies. In addition to drought, many invasive plants also tolerate some other abiotic stresses, such as UV, salinity, heat and/or cold. However, few work is reported for studies on trade-offs between resistance to insects and tolerance to these abiotic stresses. We encourage that future studies focus on the difference of defenses against insects and responses to these broad abiotic stress factors. Moreover, comparison between plants of native and introduced populations of the same invasive species may explicitly document the genetic changes of these traits.

IMPLICATIONS FOR MANAGEMENT OF INVASIVE PLANTS

Biological control of invasive plants via introduction of host-specific insects is one of the major approaches against invaders worldwide (Müller-Schärer et al. 2018; Schwarzländer et al. 2018). Invasive plants, such as A. artemisiifolia could trade-off between resistance to insects and tolerance to abiotic stresses, providing new insights into biological control (Müller-Schärer et al. 2014; Sun et al. 2022). Introduction of specialist insects from the native ranges enables invasive plants and their co-evolved enemies to reassociate, likely enhancing plant defense against insects. However, such reassociation may also result in an evolutionary decrease in abiotic stress tolerance and thus likely reduces their competitive ability compared with indigenous species. Together with the direct effects of insect damage on plant growth and reproduction, these accompanying effects on responses to abiotic stresses could enhance the efficacy of biocontrol over time (Xiao et al. 2019). Thus, simultaneously considering responses to both biotic and abiotic stress are necessary when in assessing the long-term effects of classical biological control programs.

OUTLOOKS

How plants adapt to changing environments is one of the major themes in ecology and evolution, while plant invasions provide a unique opportunity to examine plant ecological and evolutionary responses to changing biotic and abiotic environments during their invasion processes. To date, evidences showing evolutionary trade-offs between defenses to biotic and abiotic stresses in invasive plants are rare. We encourage more studies should be conducted to test whether and how invasive plants change their defense strategies to cope with the changing biotic (e.g. herbivorous insects, pathogen diseases and neighbor competitions) and abiotic (e.g. drought, UV and salinity) environments. Since chemical responses of plants to those environmental factors are one of the major responses, metabonomic approach could provide an overall view of changes in identities and amounts of primary and secondary chemicals, to reveal invasive plant’s evolutionary changes and to enable comparing metabolic profiles in relation to other factors such as abiotic environmental stresses. Moreover, transcriptomics approaches may be used to further investigate key defensive genes regulating plant responses.

Funding

This work was supported by the National Natural Science Foundation of China (U21A20190).

Conflict of interest statement. The authors declare that they have no conflict of interest.

REFERENCES