Oak genotype and phenolic compounds differently affect the performance of two insect herbivores with contrasting diet breadth

Abstract

Research on plant-herbivore interactions has long recognized that plant genetic variation plays a central role in driving insect abundance and herbivory, as well as in determining plant defense. However, how plant genes influence herbivore feeding performances, and which plant defensive traits mediate these effects, remain poorly understood. Here we investigated the feeding performances of two insect leaf chewers with contrasting diet breadth (the generalist Lymantria dispar L. and the specialist Thaumetopoea processionea L.) on different genotypes of pedunculate oak (Quercus robur L.) and tested the role of leaf phenolics. We used leaves from four clones of 30 Q. robur full-sibs grown in a common garden to estimate the performance of both herbivores in laboratory feeding trials and to quantify the concentration of constitutive chemical defences (phenolic compounds). We found that tree genetics influenced leaf consumption by T. processionea but not by L. dispar. However genetic variation among trees did not explain growth rate variation in either herbivore nor in leaf phenolics. Interestingly, all phenolic compounds displayed a positive relationship with L. dispar growth rate, and leaf consumption by both herbivores displayed a positive relationship with the concentrations of condensed tannins, suggesting that highly defended leaves could induce a compensatory feeding response. While genetic variation in oaks did not explain herbivore growth rate, we found positive genetic correlations between the two herbivores for leaf consumption and digestion. Overall, we found that oak genotype and phenolic compounds partly and independently contribute to variability in herbivore performance. We challenged the current view of plant-insect interaction and provided little support to the idea that the effect of plant genotype on associated organisms is driven by plant defences. Together, our results point to the existence of genetically determined resistance traits in oaks whose effects differ between herbivores and motivate further research on mechanisms governing oak-herbivore interactions.

Metabolomic and transcriptomic analyses of Prunus davidiana reveal the key resistance compound to green peach aphid, betulin

“…The 449 metabolites were clustered into 10 major categories (P < 0.05), including avonoids (86, ~ 19.15%), lipids (67, ~ 14.92%), phenolic acids (66, ~ 14.70%), amino acids and their derivatives (56, ~ 12.47%), organic acids (37, ~ 8.24%), nucleotides and their derivatives (36, ~ 8.02%), lignans and coumarins (18, ~ 4.01%), alkaloids (17, ~ 3.79%), terpenes (13, ~ 2.90%), and tannins (2, ~ 0.45%) (Supplementary Table 1). Several of these metabolites have been reported to play important roles in insect or disease resistance, for instance, avonoids, phenolic acids, and alkaloids [13][14][15] .…”

Tree species identity and forest composition affect the number of oak processionary moth captured in pheromone traps and the intensity of larval defoliation

“…Likewise, if masking or repellent cues are emitted by nonhosts (Zhang & Schlyter, 2004;Bruce et al, 2005;Togni et al, 2010;Bruce & Pickett, 2011;Jactel et al, 2011), their effect would have increased with their basal area, which was not the case. An alternative hypothesis is that, at the scale at which we defined species diversity, associational effects might have been mediated by changes in leaf traits relevant to OPM consumption (Damestoy et al, 2019), resulting from several mechanisms, including competition for resources or the emission of volatile compounds by neighbouring plants that change some physical and/or chemical traits of focal plant (Arimura et al, 2001;Agrawal et al, 2006;Turlings & Ton, 2006;Barbosa et al, 2009;Ballaré, 2014;Kos et al, 2015;Castagneyrol et al, 2017). It is also possible that OPM enemies were more abundant and more diverse in mixed stands, thus exerting a stronger top-down control on OPM larvae (Root, 1973;Wilby & Thomas, 2002;Sobek et al, 2009;Straub et al, 2014;Fernandez-Conradi et al, 2018).…”

“…The difference in damage between oak species could be the result of a difference in leaf quality leading to a change in the consumption rate of OPM larvae. Several studies showed a change of consumption rate with leaf quality of the host (Lazarevic et al, 2002;Foss & Rieske, 2003;Barbehenn et al, 2009;Milanović et al, 2014;Damestoy et al, 2019). However, it remains uncertain whether differences in defoliation among host species result from differences in the abundance of OPM larvae or from differences in their feeding behaviour, where larvae could compensate for lower nutritional quality by consuming more leaf material (Damestoy et al, 2019).…”

Genetic divergence along a climate gradient shapes chemical plasticity of a foundation tree species to both changing climate and herbivore damage

“…Such provenance effects are partially the product of selective environmental adaptations (Turnbull & Griffin, 1985) and have been demonstrated for multiple functional traits in numerous tree species (Abdala‐Roberts et al, 2016; Arend et al, 2011; Cooper et al, 2019; Nabais et al, 2018). Trees may also exhibit considerable variation in trait expression within provenances, as a consequence of local genetic and environmental variation (Damestoy et al, 2019; Moreira & Abdala‐Roberts, 2020; Paaso et al, 2017). Such trait differences are the product of genotypic, developmental, and microenvironmental variation, and their interactions (Westerband et al, 2021).…”