Testing the role of biotic interactions in shaping elevational diversity gradients: An ecological metabolomics approach.

Seminal hypotheses in ecology and evolution postulate that stronger and more specialized biotic interactions contribute to higher species diversity at lower elevations and latitudes. Plant-chemical defenses mediate biotic interactions between plants and their natural enemies and provide a highly dimensional trait space in which chemically mediated niches may facilitate plant species coexistence. However, the role of chemically mediated biotic interactions in shaping plant communities remains largely untested across large-scale ecological gradients. Here, we used ecological metabolomics to quantify the chemical dissimilarity of foliar metabolomes among 473 tree species in 16 tropical tree communities along an elevational gradient in the Bolivian Andes. We predicted that tree species diversity would be higher in communities and climates where co-occurring tree species are more chemically dissimilar and exhibit faster evolution of secondary metabolites (lower chemical phylogenetic signal). Further, we predicted that these relationships should be especially pronounced for secondary metabolites known to include antiherbivore and antimicrobial defenses relative to primary metabolites. Using structural equation models, we quantified the direct effects of rarefied median chemical dissimilarity and chemical phylogenetic signal on tree species diversity, as well as the indirect effects of climate. We found that chemical dissimilarity among tree species with respect to all metabolites and secondary metabolites had positive direct effects on tree species diversity, and that climate (higher temperature and precipitation, and lower temperature seasonality) had positive indirect effects on species diversity by increasing chemical dissimilarity. In contrast, chemical dissimilarity of primary metabolites was unrelated to species diversity and climate. Chemical phylogenetic signal of all metabolite classes had negative direct effects on tree species diversity, indicating faster evolution of metabolites in more diverse communities. Climate had a direct effect on species diversity but did not indirectly affect diversity through chemical phylogenetic signal. Our results support the hypothesis that chemically mediated biotic interactions shape elevational diversity gradients by imposing stronger selection for chemical divergence in more diverse communities and maintaining higher chemical dissimilarity among species in warmer, wetter, and more stable climates. Our study also illustrates the promise of ecological metabolomics in the study of biogeography, community ecology, and complex species interactions in high-diversity ecosystems.