Independent and interactive effects of plant genotype and environment on plant traits and insect herbivore performance: A meta‐analysis with Salicaceae

Abstract

Ecological research has increasingly highlighted the importance of intraspecific variation in shaping the structure and function of communities and ecosystems. Indeed, the effects of intraspecific variation can match or exceed those of interspecific variation. Previous reviews of intraspecific variation in plant traits across heterogeneous environments have focused primarily on mean phenotypic effects. We propose that a richer and fuller understanding of the ecological causes and consequences of intraspecific variation would be provided by partitioning trait variance into its subcomponents (genetic, environment, genotype by environment interaction). We used a meta‐analysis of 352 sets of genetic, environment and genotype by environment (G×E) variation estimates from 72 studies of Salicaceae to compare these sources of variation across plant traits (growth, foliar nitrogen, defence compounds), insect herbivore performance metrics (e.g., survival, growth, fecundity) and environmental conditions (e.g., soil nutrients, water, defoliation). Our findings revealed that variation in levels of defence compounds (both condensed tannins and salicinoids) and insect herbivore performance were primarily genetically determined, while variation in plant growth and foliar nitrogen was more environmentally determined. Plasticity in plant growth, foliar nitrogen levels and insect herbivore performance varied substantially across different sites (year × location), and nutrient, water and carbon dioxide environments. Plasticity was lowest for chemical defence traits and all traits in contrasting ozone and defoliation environments. Our quantitative review also revealed several gaps in the literature, including a need for surveying more mature plants, a wider variety of insect herbivore species (e.g., leaf‐galling insects, specialist insects) and underrepresented environmental treatments (e.g., competition, defoliation, disease, light and water availability). Findings from this analysis highlight the importance of, and patterns within, intraspecific variation with respect to shaping the evolvability and plasticity of traits and governing the interactions of plants and insects. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13249/suppinfo is available for this article.

Host plant phenology, insect outbreaks and herbivore communities – The importance of timing

“…The lack of an effect of host plant genotype on our specialized herbivore insect community could be a results of specialized herbivores being less influenced by plant genotype than generalists (Barker, Holeski, & Lindroth, ). Previous studies have revealed host genotype as a weak predictor of species richness in our study system (Pohjanmies et al, ; Tack, Ovaskainen, Pulkkinen, & Roslin, ), although the genetic diversity of host plants has been shown to affect herbivore abundances (Pohjanmies et al, ).…”

“…The only effect detected was that of plant phenology, suggesting that differences between early and late trees will persist into the future. In a recent meta‐analysis, Barker et al () found that most phenotypic variation in several plant traits of the Salicaceae family was explained by genotype and environment individually, whereas little variation was explained by the G x E interaction. In fact, they found that plant genotype had a big impact on insect herbivore performance.…”

Climate and host genotype jointly shape tree phenology, disease levels and insect attacks

“…Plant genotype is an additional strong driver of disease and insect dynamics in wild and agricultural systems (Flor 1955, Whitham et al 2008, Laine 2011, Busby et al 2014, Burdon and Laine 2019. As one mechanism, plant genotypes can vary greatly in chemical defense compounds and, subsequently, in their susceptibility to different herbivores (Service 1984, Donaldson and Lindroth 2007, Johnson 2008, Barker et al 2019. Overall, we still lack insights in the joint impact of climate and plant genetics on the seasonal dynamics of plant-attackers (e.g.…”

Chemical defense over decadal scales: Ontogenetic allocation trajectories and consequences for fitness in a foundation tree species

“…This difference in patterns could be a consequence of examining trait correlations within a single year in previous studies (Cole et al, ; Stevens & Esser, ) versus across many years in our study. In addition, environmental variation strongly influences both growth and CT concentrations in aspen (Barker, Holeski, & Lindroth, ; Osier & Lindroth, ) so the relationship between growth and CTs is context‐specific and thus may vary among studies.…”

“…In contrast, the roles of CTs in conferring resistance is less clear, but the compounds may increase tolerance in defoliated trees by enhancing N uptake from litter and herbivore frass (Madritch & Lindroth, ). Finally, CT expression is highly plastic and responsive to resource availability, which may attenuate costs compared with more genetically determined, resource‐independent SPG expression (Barker et al, ; Donaldson & Lindroth, ; Osier & Lindroth, ). The modest negative correlation between SPGs and CTs in mature trees ( F 1,108 = 53.5, p < .001, r = −.58; data not shown) does, however, complicate comparisons of results for the two defenses.…”