Plant scent and plant–insect interactions—Review and outlook from a macroevolutionary perspective

Abstract

The astonishing diversity of plants and insects and their entangled interactions are cornerstones in terrestrial ecosystems. Co-occurring with species diversity is the diversity of plant secondary metabolites (PSMs). So far, their estimated number is more than 200 000 compounds, which are not directly involved in plant growth and development but play important roles in helping plants handle their environment including the mediation of plant-insect interactions. Here, we use plant volatile organic compounds (VOCs), a key olfactory communication channel that mediates plant-insect interactions, as a showcase of PSMs. In spite of the cumulative knowledge of the functional, ecological, and microevolutionary roles of VOCs, we still lack a macroevolutionary understanding of how they evolved with plant-insect interactions and contributed to species diversity throughout the long coevolutionary history of plants and insects. We first review the literature to summarize the current state-of-theart research on this topic. We then present various relevant types of phylogenetic methods suitable to answer macroevolutionary questions on plant VOCs and suggest future directions for employing phylogenetic approaches in studying plant VOCs and plant-insect interactions. Overall, we found that current studies in this field are still very limited in their macroevolutionary perspective. Nevertheless, with the fast-growing development of metabolome analysis techniques and phylogenetic methods, it is becoming increasingly feasible to integrate the advances of these two areas. We highlight promising approaches to generate new testable hypotheses and gain a mechanistic understanding of the macroevolutionary roles of chemical communication in plant-insect interactions.

Field sampling of fig pollinator wasps across host species and host developmental phase: Implications for host recognition and specificity

“…For plant–pollinator relationships an increasing number of studies suggest that similar volatiles attract similar pollinators (Burkle & Runyon, 2019 ; Hetherington‐Rauth & Ramírez, 2016 ; Huang et al, 2015 ; Stökl et al, 2005 ). As with other plant groups, fig volatiles may be phylogenetically constrained (Joffard et al, 2020 ; Schwery et al, 2022 ). The degree to which different levels of phylogenetic distance predicts similarity of chemical cues should correspond to particular pollinator species being more likely to shift within fig sections or subgenera than between them (Cook & Segar, 2010 ).…”

“…For plant-pollinator relationships an increasing number of studies suggest that similar volatiles attract similar pollinators (Burkle & Runyon, 2019;Hetherington-Rauth & Ramírez, 2016;Huang et al, 2015;Stökl et al, 2005). As with other plant groups, fig volatiles may be phylogenetically constrained (Joffard et al, 2020;Schwery et al, 2022). The degree to which different levels of for many herbivorous insect groups (Becerra, 1997;Erbilgin et al, 2014;Murphy & Feeny, 2006;Rigsby et al, 2017).…”

Chemical communication between plants and insects

“…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).…”

“…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 convergence in phytochemistry and flower–insect visitor interactions along an Andean elevation gradient

“…The hypotheses of phylogenetic constraint versus ecological convergence represent two theoretical extremes; the reality is likely an intermediate dynamic in which both processes shape floral fragrance (Raguso, 2008 ; Schwery et al, 2023 ). While some comparative studies have found phylogenetic structuring of floral scents (Azam et al, 2013 ; Steiner et al, 2011 ), others have found floral scent divergence driven by local biogeographic differences (Moré et al, 2021 ).…”