A scale-dependent framework for trade-offs, syndromes, and specialization in organismal biology.

Biodiversity is defined by trait-differences between organisms, and biologists have long sought to predict associations among ecologically important traits: why do some traits trade off while others are co-expressed? Why might some trait associations hold across levels of organization, from individuals and genotypes to populations and species, while others only occur at one level? Understanding such scaling is a core biological problem, bearing on the evolution of ecological strategies as well as forecasting responses to environmental change. Explicitly considering the hierarchy of biodiversity and expectations at each scale (individual change, evolution within and among populations, and species turn-over) is necessary as we work towards a predictive framework in evolutionary ecology. Within species, a trait may have an association with another trait due to phenotypic plasticity, genetic correlation, or population-level local adaptation. Plastic responses are often adaptive and yet individuals have a fixed pool of resources; thus, positive and negative trait associations can be generated by immediate environmental needs and energetic demands. Genetic variation and covariation for traits within a population are typically shaped by varying natural selection in space and time. Although genetic correlations are infrequently long-term constraints, they may indicate competing organismal demands. Traits are often quantitatively differentiated (local adaptation) among populations, although selection rarely favors qualitatively different strategies until populations become reproductively isolated. Across species, niche specialization to particular habitats or biotic interactions may determine trait correlations, a subset of which are termed "strategic trade-offs" because they are a consequence of adaptive specialization. Across scales, constraints within species often do not apply as new species evolve, and conversely, trait correlations observed across populations or species may not be reflected within populations. I give examples of such scale-dependent trait associations and their causes across taxonomic groups and ecosystems, and in the final section of the paper I specifically evaluate leaf economic spectrum traits and their associations with plant defense against herbivory. Scale-dependent predictions emerge for understanding plant ecology holistically, and this approach can be fruitfully applied more generally in evolutionary ecology. Adaptive specialization and community context are two of the primary drivers of trade-offs and syndromes across biological scales.