Environmental gradients and the evolution of tri‐trophic interactions

Abstract

Long‐standing theory predicts herbivores and predators should drive selection for increased plant defences, such as the specific production of volatile organic compounds for attracting predators near the site of damage. Along elevation gradients, a general pattern is that herbivores and predators are abundant at low elevation and progressively diminish at higher elevations. To determine whether plant adaptation along such a gradient influences top‐down control of herbivores, we manipulated soil predatory nematodes, root herbivore pressure and plant ecotypes in a reciprocal transplant experiment. Plant survival was significantly higher for low‐elevation plants, but only when in the presence of predatory nematodes. Using olfactometer bioassays, we showed correlated differential nematode attraction and plant ecotype‐specific variation in volatile production. This study not only provides an assessment of how elevation gradients modulate the strength of trophic cascades, but also demonstrates how habitat specialisation drives variation in the expression of indirect plant defences.

Plant adaptation to different climates shapes the strengths of chemically mediated tritrophic interactions

“…VOCs for attracting predators) than in direct resistance. In a previous study, we showed that F. rubra ecotypes attracting more EPNs in olfactometers were those also surviving the best in the field, under herbivory (Kergunteuil, Röder, et al, ). Investment in attractive VOC blend production seems thus an efficient strategy for warding off herbivores, even when direct resistance is impaired.…”

“…Specifically, Dobzhansky () postulated that the intensity of biotic interactions increases at the warmer and more stable tropical latitudes and this in turn should select for higher values of traits mediating these interactions (Schemske, Mittelbach, Cornell, Sobel, & Roy, ). Accordingly, tropical (Bolser & Hay, ; Coley & Aide, ; Coley & Barone, ; Moles, Wallis, et al, ; Rasmann & Agrawal, ) and low‐elevation (Dostálek et al, ; Kergunteuil, Röder, & Rasmann, ; Pellissier, Roger, Bilat, & Rasmann, ; Scheidel & Bruelheide, ; Zehnder et al, ) plants should be selected for producing higher values of defence‐related traits. Nonetheless, exceptions from this pattern exist (Moles, Bonser, Poore, Wallis, & Foley, ; Moles, Wallis, et al, ).…”

“…While the production of secondary metabolites, such as VOCs, is highly dependent on the genetic make-up of plants, or the type of herbivore attacking the plants, their production is also influenced by abiotic factors such as temperature and humidity (Gouinguené & Turlings, 2002). Along elevation gradients, for instance, the diversity and abundance of VOCs have been shown to vary strongly between low-and high-elevation adapted ecotypes (Kergunteuil, Röder, et al, 2019) or species (Defossez, Pellissier, & Rasmann, 2018). Therefore, elevation patterns in plant defences are tightly bound to variations in climatic conditions per se.…”

“…For instance, the observations that climatic conditions imposing slow growth (e.g. in cold habitats) select for higher levels of defences have been mainly highlighted when comparing species (Defossez et al, 2018;Fine, Mesones, & Coley, 2004), but not when analysing intraspecific variation (Kergunteuil, Röder, et al, 2019;Pellissier et al, 2014), in which a decline in defence in colder habitats has been mostly associated with lower herbivore pressure (Kergunteuil, Röder, et al, 2019;Pellissier et al, 2014).…”

Tri‐trophic interactions: bridging species, communities and ecosystems

“…Determining the sources of variation will thus require combining environmental manipulations with reciprocal transplant experiments, possibly complemented by genomic approaches to determine the genetic bases for trait variation, patterns of gene expression, as well as manipulations of relevant traits. Third, studies of environmental gradients must move beyond characterising individual food chains (reviewed by Moreira et al ; Defossez et al ; Kergunteuil et al ) to explicitly characterise and compare multiple, co‐occurring tri‐trophic food chains. This approach is analogous to other trait‐based approaches ( sensu McGill et al ), but with a simultaneous focus on plants, herbivores, and natural enemies as well as traits relevant to TTIs (e.g.…”