Plant volatile defenses rather than non-volatile defenses mediate evolutionary interactions between plants and tephritid flies

This blog post is provided by Hua Wang and tells the #StoryBehindThePaper for the article “Plant volatiles mediate evolutionary interactions between plants and tephritid flies and are evolutionarily more labile than non-volatile defenses”, which was recently published in Journal of Animal Ecology.

Why do I study the relationship between plants and flies? Even before starting my PhD research, I have known of and been fascinated by the bipartite relationship between species in the family Asteraceae and species of tephritid flies, which is investigated in Prof. Sun’s laboratory. This bipartite structure emerges because of the relationships between species density and functional traits, e.g., plant inflorescence (capitulum) size and fly body size. However, our research has shown that other factors are also extremely important. My research has shown that specific fly species do not necessarily use all plant species with similar capitulum sizes. After reviewing the literature, I proposed that chemical defenses might mediate the interaction between plants and flies. Prof. Sun encouraged me to think more about the proposal, and we finally decided to ask whether plant phylogeny or chemical defenses (including both volatile and non-volatile chemicals) has a greater influence on the plant-fly relationships.

Our field studies were carried out on the eastern Qinghai-Tibet Plateau, with an altitude of 3500 m. I worked in this location for four months from June to September from 2017 to 2019, investigating the plant community, measuring plant capitula, and collecting volatile chemicals from capitula. It was an arduous but very exciting time for me. I had acute altitude sickness at the beginning and often experienced rapid heart beating, especially on rainy days. My face was also getting sunburned, even though I always wore a large hat. Nevertheless, Prof. Sun’s laboratory group provided me with much support and encouragement. I have nearly 10 academic “sisters and brothers” who worked with me and I really enjoyed my time on the plateau.

My academic sister (left) and I (right) are investigating plant communities (Photo: Hua Wang)

Asteraceae species are diverse (>40 species) and abundant in the alpine meadow on the eastern Tibetan Plateau, and they often suffer very high pre-dispersal seed predation from more than 20 Tephritid fly species. Female flies puncture developing capitula using ovipositors and deposit eggs, and the larvae grow and develop by consuming developing seeds. The larvae cannot move between capitula before they emerge as adults. I collected capitula and determined the feeding relationship between plants and flies, which constitute a bipartite network. I wondered whether the plants and flies are phylogenetically related and whether plant defensive chemical traits mediate the evolutionary interaction between plants and flies. To address these questions, I investigated the effects of plant chemical defenses and phylogeny on plant-herbivore interactions.

Fig. 1 The Plant-fly bipartite network. (tephritid flies: Tephritis femoralis, Campiglossa nigricauda, Oedaspis sp1, Terellia megalopyge, C. flavescens, Asteraceae plants: Saussurea nigrescens, Anaphalis flavescens, Leontopodium franchetii, Cremanthodium brunneopilosum, L. souliei, Aster diplostephioides, S. stella). Image contributors: the tephritid flies: Xinqiang Xi; the Asteraceae plants: Hua Wang

This work is now published in a recent paper in the Journal of Animal Ecology, and reveals a highly resolved bipartite trophic network consisting of 17 host species and 20 tephritid fly species. I constructed phylogenetic trees for 17 plant species and 20 tephritid fly species, identified the secondary metabolites (both volatiles and non-volatiles) of 17 plant species, and measured their relative contents. We found that interspecific similarity in volatiles—but not non-volatiles and phylogenetic distance—significantly accounted for the herbivore community across the plant species. This research indicates that plant volatiles—but not non-volatile compounds and species identity—dictate plant-tephritid fly interactions. Moreover, we observed a strong phylogenetic signal for non-volatiles but not for volatiles. These results indicate that closely related herbivores do not necessarily use closely related host species with similar non-volatiles, but rather tend to attack plants producing similar volatiles. Thus, plant volatiles are evolutionarily more labile than non-volatiles, and herbivore traits associate with host use. As a result, the interactions between plants and herbivores are evolutionary asymmetric, such that plant volatiles play an important role in plant-herbivore interactions.

Video of Terellia megalopyge depositing eggs on the capitula of Saussurea nigrescens. (Video: Xinqiang Xi)

Insect offspring success should depend on both volatiles (preference) and non-volatiles (performance) for their survival, growth, and development, and hence both plant chemical profiles may evolutionarily affect host-use. However, herbivores with mobile versus immobile larvae may depend differentially on host volatile versus non-volatile compounds. Herbivores with mobile larvae predominantly use visual and olfactory traits to locate potential hosts, and subsequently use gustatory factors to decide whether or not to use the host. In contrast, herbivores with immobile larvae depend heavily on visual and olfactory traits to search and locate potential hosts, and then use olfactory, chemical, and tactile traits (located at the end of ovipositors) to decide whether or not to use a host. In either case, the tephritid flies in our study cannot “taste” the non-volatile compounds within developing seeds. Indeed, there are no developing seeds because these flies lay eggs before flowering. Therefore, it is reasonable to assume that plant volatiles rather than non-volatiles determine plant-herbivore interactions.

In addition, because plants are under intense selection pressure resulting from herbivores and to avoid sharing enemies with neighboring plants, they change their volatile profiles. We suggest that the rapid acquisition of differences in chemical defense traits among closely related plants might increase plant fitness and foster species coexistence.

Bio: My name is Hua Wang. I am a PhD student studying in the laboratory of Prof. Shucun Sun, School of Life Science at Nanjing University. My PhD research focuses on the role of plant chemical defenses in plant-herbivore interactions.

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