Chemical communication between plants and insects

Abstract

The chemical communication between plants and insects plays a pivotal role in shaping plant–insect interactions and ecological networks, making it a vital component in both natural and agricultural ecosystems. Despite the considerable advancements in the field of chemical ecology (Meinwald & Eisner, 2008), numerous challenges remain due to its interdisciplinary nature (encompassing evolutionary biology, neurobiology, chemistry, animal behavior, and network ecology), as well as the complexity of chemical communication (including mediating mutualistic and antagonistic relationships, and multifunctional roles at the community level). In this special issue of the Journal of Systematics and Evolution, we present a collection of 10 papers addressing these challenges through original research and comprehensive reviews of relevant subfields. The contributions can be organized into four primary themes: (i) community-level communication theory (Zu et al., 2022) and its application to plant–pollinator communities (Yang et al., 2022); (ii) the evolutionary history of communication from a phylogenetic and macroevolutionary perspective (Martel et al., 2021; Schwery et al., 2022); (iii) various communication types, including plant–pollinator (Martel et al., 2021), plant–pest (Fang et al., 2023), and plant–fungi–insect interactions (Xu et al., 2023); and (iv) an exploration of different communication factors such as distyly (Zeng et al., 2022), odor dynamics (Feng et al., 2022), chemical structures (Zhang et al., 2022), and the impact of herbicides (Ramos et al., 2022).

Ecological communities are characterized by complex interaction networks involving numerous interdependent species. However, traditional studies of plant–insect chemical communication have primarily focused on specific species, with only a few links between plant–insect interactions. With the rapid development of chemical collection instruments, there has been a growing interest in community-level studies on plant–insect chemical communication (reviewed by Zu et al., 2022). This development highlights the need for a conceptual framework and practical methodologies to expand our mechanistic understanding of plant–insect chemical communication from pairwise species interactions to ecological network levels.

Zu et al. (2020) proposed an innovative approach by incorporating Shannon information theory (Shannon, 1948), originally developed for telecommunication, into the study of plant–insect communication. In this special issue, Zu et al. (2022) contribute a perspective paper outlining the fundamentals of information theory and its application in studying the patterns and processes of cross-species chemical communication from both top-down and bottom-up perspectives. Shannon information theory emphasizes the syntactic aspect (statistical structure) rather than the semantic aspect (content and meaning) of information. It defines information as the reproducibility of a message from one end to another, allowing for the calculation of communication clarity (information) or ambiguity (entropy) based on probability distributions. Zu et al. (2020, 2022) introduced the concept of “information fitness” to describe the evolutionary processes of emitters and receivers in plant–insect chemical communication within the information landscape. In a plant–herbivore network, their antagonistic relationship suggests conflicting information processes (information arms race), where plants aim to maximize herbivore decoding uncertainty while herbivores strive to minimize decoding uncertainty (Zu et al., 2020). In contrast, plant–pollinator networks involve mutualistic relationships, with pollinators seeking to minimize decoding uncertainty to locate floral resources. Plants, however, must balance minimizing uncertainty for their mutualistic pollinators while preventing antagonistic parties from eavesdropping on the information. Yang et al. (2022) examined this scenario in a fig–fig wasp network system, finding that the empirical communication structures were accurately represented only when considering plants’ dual objectives of attracting mutualists and confusing antagonists. This integration of information theory into plant–insect communication research holds great potential for advancing our understanding of community-level network coevolution (Sole, 2020).

Plants and insects have evolved together for hundreds of millions of years (Ehrlich & Raven, 1964). The evolutionary history of species can affect their interactions, adaptations, and diversification. Therefore, macroevolutionary studies, which consider evolutionary history using phylogenetic approaches, offer valuable insights into plant chemicals and plant–insect interactions. Schwery et al. (2022) provide a comprehensive review and outlook from the macroevolutionary perspective, focusing on volatile organic compounds (VOCs), the key chemical group mediating plant–insect olfactory communication. It has been suggested that plants produce more than 1700 flower volatiles (Knudsen et al., 2006; Farré-Armengol et al., 2020), and insects have a relatively large portion of olfactory receptor genes in their genomes that enable them to discriminate numerous and complex olfactory signals (reviewed by Khallaf & Knaden, 2022). Schwery et al. found that among the more than 3000 publications on plant scent and plant–insect interactions, only 65 papers met the evaluation criteria. Topic-wise, most of the 65 papers focused primarily on plants (instead of insects), the attraction roles of VOCs (instead of the deterring roles), and on taxonomic groups of related species (instead of cooccurring species in communities). Methodology-wise, the majority of the studies employed phylogenetic approaches to test phylogenetic signals in plant VOCs (whether closely related species produce similar VOCs due to their relatedness and shared evolutionary history) and trait evolution (e.g., which traits are ancestral and how fast traits evolve). To make the methods more accessible for wide audiences, Schwery et al. went on to explain different approaches suited to tackle various evolutionary questions, gave relevant published examples of their use, and highlighted useful phylogenetic software and tools (e.g., R packages). Furthermore, they also include some exciting new approaches that are currently under development (e.g., Hardenberg & Gonzalez-Voyer, 2013; Tarasov et al., 2019), for example, the trend of moving from correlational to causational inference in many fields (Verma & Pearl, 1990; Shipley, 2016; Saavedra et al., 2022). These new possibilities may revolutionize our understanding of chemical communication in plant–insect interactions.

In addition to the review and perspective paper, Martel et al. (2021) provided a nice case study on chemical trait evolution in the orchid genus Neotinea. Floral chemicals can play important roles in pollinator shifts and plant diversification even without changes in morphology (e.g., Shuttleworth & Johnson, 2010). All the Neotinea species are deceptive, with Neotinea ustulata attracts specialized pollinators of the tachinid flies (mostly males). Martel et al. (2021) found that N. ustulata has evolved a unique floral cuticular chemical composition featured with two floral cuticular alkenes in high relative quantities. These cuticular hydrocarbons are like insect sex pheromones and stimulate electrophysiological responses of tachinid antennae. By further mapping the production and concentration of these two cuticular alkenes in the tribe Orchidinae and the corresponding pollinators for each of the species, they suggested that bee pollination and the absence of the two cuticular alkenes were the ancestral states in the tribe. It is an evolutionary exaptation in N. ustulata to evolve with the high relative quantities of the two cuticular alkenes, and tachinid fly pollination was a unique evolutionary innovation for N. ustulata.

Chemical communication is an ancient and ubiquitous channel of communication, suggesting its potential roles in a wide range of interactions within and between species, as well as across multiple species. For example, cuticular hydrocarbons not only play important roles in plant–pollinator interactions as shown by Martel et al. (2021), but are also crucial for within species communications of insects. Fang et al. (2023) studied different cuticular hydrocarbons and their roles for sex recognition in juniper bark borers Semanotus bifasciatus. This longhorned beetle causes severe damage to some tree species. Fang et al. found that in this beetle species, the cuticular hydrocarbons emitted by males and females are qualitatively the same, but quantitatively different. Using bioassays, they further showed that three cuticular hydrocarbons are functional for sex recognition and whether the mixture will trigger more mating attempts for either sex depends on the ratios of the three compounds (female-specific or male-specific ratios). The sex-dependent elicitation can help us to better design useful tools for pest control.

In another paper, Xu et al. (2023) reviewed chemical communications in plant–fungi–insect interactions, an important but understudied cross-kingdom tripartite communication type. They summarized various plant-associated fungi and their influences on plant–insect interactions. For example, chemicals from plant-associated fungi can have direct effects on plant–insect interactions; or indirect effects by modifying host plant metabolites and further modulate plant–insect interactions. These tripartite interactions have multiple ecological implications, including decomposition, pollination, herbivory, and the spread of disease in agricultural and forestry crops associated with pathogenic fungi. They further highlighted that due to the complex nature of chemical blends and their interdependent roles in mediating complex interactions, more mechanistic studies are needed in the future to decipher the multifunctional roles of the infochemicals in both experimental settings and natural conditions.

The production of plant volatiles is heritable (Zu et al., 2016) and also strongly influenced by biotic and abiotic environment factors (e.g., Schiestl & Ayasse, 2001; Majetic et al., 2009). Consequently, a variety of factors can contribute to diverse and dynamic plant volatiles, affecting their functionality in communication. For example, Feng et al. (2022) investigated the production rhythms of floral scent and nectar associated with floral color change in Lonicera japonica, in Caprifoliaceae. A total of 34 compounds were detected in the flowers of this species and total scent emission was significantly higher in the second night than at other times. The scent emission of three major compounds, Linalool, cis-3-Hexenyl tiglate, and Germacrene D was also significantly higher in the second night, but the relative content of Linalool decreased gradually, cis-3-Hexenyl tiglate increased gradually, and the relative content of Germacrene D did not differ among different flowering times. The floral scent rhythms in different flowering times did not match the color change and nectar secretion, suggesting that floral color (visual) and scent (olfactory) in this species may play different roles in attracting or filtering various visitors.

Moreover, the floral scent variation can be associated with intraspecific mating system transitions. For example, the breakdown of distyly to homostyly represents a classic example of a shift from outcrossing to selfing in the genus Primula. Zeng et al. (2022) detected significant variation of VOCs among populations of Primula oreodoxa. The floral VOCs from the homostylous and distylous (long- or short-styled) morphs differ in both emission rate and composition. Specifically, homo- and di-stylous morphs can be distinguished by 12 compounds, mainly monoterpenoids and sesquiterpenoids. Of these compounds, (E)-β-Ocimene was the most important one in contributing to the difference in volatiles, with significantly lower emissions in homostyles. This result supported the hypothesis that the transition from outcrossing to selfing is accompanied by the loss of floral volatiles and the modification to floral fragrances in P. oreodoxa associated with mating system change through relaxed selection for floral attractiveness in homostylous populations.

The subtler differences in conformational changes and functional diversity of odors could make the communications of animals and plants more complicated. Lianlool as a representative compound that exhibits obviously multifunctional characteristics actually exists as two enantiomeric isomers in nature, and both enantiomers occur randomly and disproportionately across plant species (Raguso, 2016). Based on the literature, Zhang et al. (2022) summarized the biosynthesis and transcriptional regulation of terpenoids including Lianlool, and then focused on the biological function of linalool in plant–insect interactions. They found that flowers emitting linalool as the dominant volatile appeal to broad assemblages of pollinators, especially moths and bees are the main pollinators of Linalool- dominant flowers. The two enantiomers of linalool have distinct functions. (S)-(+)-Linalool mainly attracts pollinators, while (R)-(−)-Linalool seems to act as insect repellent. Thus, Zhang et al. (2022) suggested that further research on the biofunctional diversity and genetic mechanisms behind linalool enantiomers could contribute to unveiling the complexity of plant survival strategies. Additionally, it could provide a theoretical foundation and practical basis for understanding the existence and directional transformation of enantiomeric isomers in plants.

The delicate natural ecological interactions between plants and insects can be indirectly impacted by a global increase in intensive agriculture and availability of herbicide-resistant crops through habitat degradation and climate change (Soroye et al., 2020; Wagner et al., 2021; Zattara & Aizen, 2021). Considering the herbicides interfere with biosynthetic pathways and phytohormones involved in the production of several classes of plant volatiles that mediate plant–insect chemical communication, Ramos et al. (2022) argue that the exposure to sublethal herbicide doses has the potential to alter plant–insect interactions as a result of disruptions in their chemical communication. After discussing how target-site (disruptors of primary metabolism) and non-target-site (synthetic auxins) herbicides could alter the production of plant volatiles and disrupt plant–insect chemical communication, Ramos et al. (2022) proposed that research avenues to fill in the current gap in our knowledge that might derive recommendations and applied solutions to minimize herbicide impacts on plant–insect interactions and biodiversity.