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

Objective

• Investigate how genetic and phenotypic variation in trembling aspen (Populus tremuloides) influences the composition and structure of canopy insect communities.
• Identify specific genes and plant traits that shape associated insect communities, connecting intraspecific plant variation to community- and ecosystem-level patterns.

Key Findings

1. Community Genetics and Extended Phenotypes

• Intraspecific (within-species) variation in plant traits can have significant community and ecosystem impacts.
• The effects of plant genotypes on ecological communities are termed extended phenotypes.

2. Study Design

• Conducted in a common garden experiment with 1,568 aspen trees (492 genets) in Wisconsin, representing natural genetic variation.
• Surveys of over 640,000 insect individuals representing 18 common species over two years.
• Measured heritability of 13 tree traits (e.g., size, chemical defenses, phenology, morphology, reproduction).

3. Heritability of Insect Communities

• Insect community composition (which species were present) was substantially heritable; abundance and diversity metrics were less so.
• Heritability was highest for specialist leaf-modifying insects (e.g., gallers, miners, rollers).
• On average, 28% of variation in community composition was explained by aspen genotype.
• The most heritable species included Harmandia sp., Coleophoridae sp., Zeugophora scutellaris, Phyllocolpa sp., and Chaitophorus populicola.

4. Heritability and Variation of Aspen Traits

• Most aspen traits (e.g., condensed tannins, secondary metabolites, budbreak timing, flower production, extrafloral nectaries) were highly heritable (H² > 0.5).
• Phenotypic traits such as tree size, chemistry, and phenology varied substantially among genotypes.

5. Plant Traits Shape Insect Communities

• Tree size was the strongest predictor of insect species richness and abundance.
• Condensed tannin concentration negatively affected overall insect diversity, especially for leaf-modifying insects.
• Salicinoid phenolic glycosides (defensive compounds) showed positive associations with certain specialist insects, suggesting adaptation.
• Leaf traits and flower production also influenced specific insect occurrences.
• Phenology (budbreak timing) had strong effects on certain insects.

6. Genomic Associations

• 73 genes identified as associated with tree traits linked to insect communities.
• 15 genes directly associated with insect community composition (identified via SNP associations).
• Functions of some putative genes related to vacuolar functioning, cell wall structure, cellular transport, programmed cell death, and flowering time.
• No significant gene associations with overall community richness/diversity; gene effects were trait- and species-specific.
• Additional indirect evidence suggests more genes with small effects remain unidentified.

7. Genetic Mechanisms Explained via Plant Traits

• When aspen traits were included in models, detected gene effects on insect communities disappeared, indicating phenotypes mediate genetic effects on communities.

Broader Implications

• Genetic and phenotypic diversity within a foundation species (aspen) profoundly shapes associated insect communities.
• Understanding these mechanisms can inform conservation and management strategies to maintain resilient and diverse ecosystems.
• Extended phenotype concept is supported: single tree genes can affect higher-level community structure.

Methodological Advances

• Novel genomic association methods (improved mixed-effects models; accounting for genetic, phenotypic, and environmental correlations) increase confidence in findings.
• Highlights the complexity of plant-insect-genome interactions, often mediated by many genes with small effects.

Summary Table of Study Flow

| Aspect | Details | |-|--| | Population | 1,568 aspen trees, 492 genets, Wisconsin common garden | | Insect Sampling | 4 surveys over 2 years, >640,000 individuals, focus on 18 common species | | Plant Traits Measured | 13 traits across growth, defense, phenology, morphology, reproduction | | Genetic Data | 113,674 SNPs via sequence capture genotyping | | Key Analyses | Heritability partitioning, mixed-effects modeling, genomic association, multivariate stats |

Key Terms

• Heritability (H²): Proportion of phenotypic variance explained by genetic variance.
• Genet: A genetically unique individual (clone) in a population.
• Extended Phenotype: Effects of an organism's genes on its environment and associated communities.
• Specialist/Generalist: Insect species with a narrow/broad host range.

Conclusions

• Aspen extended phenotypes are strongly heritable and linked to genetic variation.
• Specific plant traits and genes can predict the structure and composition of dependent insect communities.
• The genes-to-ecosystems paradigm is supported, with plant genomic variation shaping ecological processes at higher organizational levels.

For full methodological details, gene lists, data, and analysis scripts, see supplementary and Dryad links provided in the article.