Canopy insect communities are shaped by the genes and phenotypes of their aspen hosts

The study demonstrates that plant genomic variation can propagate through phenotypes to shape not only direct interactions but also higher-level community structure, supporting the integrative genes-to-ecosystems framework in ecology.

The main objective was to identify how variation in the genes and phenotypes of trembling aspen (Populus tremuloides) influences the structure and diversity of associated canopy insect communities, and to determine if specific genetic and phenotypic mechanisms underlie those ecological relationships.

Heritability was measured by partitioning variance components in random effects regression models, comparing the proportion of variance explained by aspen genotype to total variance for both aspen traits (phenotypes) and insect community metrics (extended phenotypes).

Four traits were highly heritable: salicinoid phenolic glycoside concentration (SPG), extrafloral nectary density (EFN), budbreak timing, and flower production, with broad-sense heritability values (H^2) between 0.50 and 0.67.

The incidence (presence/absence) of several specialist insects, particularly leaf-modifying species such as Harmandia sp., Coleophoridae sp., Zeugophora scutellaris, Phyllocolpa sp., and Chaitophorus populicola, was highly heritable, with H^2 values ranging from 0.53 to 0.88.

No, diversity and abundance metrics of insect communities, such as species richness and evenness, were weakly heritable, with genotype accounting for only about 7% of the variation in diversity metrics.

Tree size (basal area, BAsqrt), budbreak timing, salicinoid phenolic glycoside concentration (SPG), and condensed tannin concentration (CT) were the most influential, collectively accounting for over 80% of the explained variation in insect community structure.

Redundancy analysis and PERMANOVA showed that aspen traits explained 17-21% of the total variation in insect community composition, with tree size being the most important single trait, followed by budbreak timing, SPGs, and CTs.

Leaf-modifying specialist herbivores, such as gallers, miners, and rollers, showed the highest heritability in their occurrence among aspen genets.

As expected, condensed tannin (CT) concentrations were negatively correlated with species richness and abundance of leaf-modifying insects, but surprisingly, increased SPG concentrations were associated with increased incidence of some specialist insects, suggesting adaptation.

Yes, 15 genes (associated with 17 SNPs) were directly linked to insect community composition metrics, mainly affecting the incidence of certain specialist insect species.

No, when models included aspen phenotypic traits as covariates, there were no significant direct genomic associations with insect incidence, suggesting that the effects of genes are mediated through tree phenotypes.

By demonstrating how genetic variation within aspen drives trait variation that in turn shapes insect communities, the study highlights the importance of genes-to-ecosystems connections for biodiversity, ecosystem resilience, and conservation planning.

Coleophoridae sp., Nematus sp., Harmandia sp., Phyllocolpa sp., and Chaitophorus populicola showed patterns indicating additional, undetected genomic associations with their incidence on aspen.

Heritability of insect incidence was highest for specialist and physically intimate feeders (such as gallers and leaf-modifiers), and lowest for free-feeding and generalist insects.

No significant gene set enrichment was detected for functional groupings of genes affecting aspen phenotypes or insect community traits.

Ontogenetic changes, such as increased size, reproductive maturity, and shifts in chemistry (e.g., lower secondary metabolites, higher nitrogen), altered which insects were common, emphasizing the importance of tree developmental stage in shaping extended phenotypes.

Extrafloral nectary density increased the incidence of only one specialist insect and negatively influenced some others (e.g., Cicadamorpha), but was not associated with common ant natural enemies in this system.

Understanding the genetic basis for trait-mediated community assembly may help managers select aspen populations with genetic compositions that promote stable, resilient, or pest-resistant ecosystems.

Despite substantial genetic and phenotypic effects, most community variation remains unexplained by tree traits, implying strong roles for environmental variation, insect population dynamics, interactions with natural enemies, and abiotic factors.

The study demonstrates that plant genomic variation can propagate through phenotypes to shape not only direct interactions but also higher-level community structure, supporting the integrative genes-to-ecosystems framework in ecology.

The main objective was to identify how variation in the genes and phenotypes of trembling aspen (Populus tremuloides) influences the structure and diversity of associated canopy insect communities, and to determine if specific genetic and phenotypic mechanisms underlie those ecological relationships.