Abiotic stress rather than biotic interactions drives contrasting trends in chemical richness and variation in alpine willows

Abstract

Plants produce an astonishing diversity of specialized metabolites as defences against herbivores, pathogens or detrimental abiotic conditions. Plants growing at different elevations are exposed to different biotic and abiotic conditions and typically show pronounced differences in their chemistry. Understanding how these differences arise through changes in various measures of chemical diversity can inform us concerning factors that contribute to the variety of metabolites found among plants. We focused on elevational changes in concentration, richness and intra‐ and interspecific variation in specialized chemistry in willows (Salix, Salicaceae) and compare them among metabolite classes with different functions. We aim to show how these various measures of chemical diversity change with elevation to reveal trends contributing to changes in plant chemistry along major ecological gradients. We studied chemistry, herbivory and fungal pathogen damage in an assemblage of seven willow species along an elevational gradient in the Alps (800–2600 m a.s.l.). We examined trends in chemical diversity using untargeted metabolomics, and further quantified trends in three specific classes: proanthocyanidins and salicinoids involved in biotic interactions, and flavonoids involved mainly in abiotic protection. We use measures of willow chemistry that take structural relatedness of metabolites into account to show if the roles of structurally distinct metabolites change with elevation. Willows from low elevations exhibited greater proanthocyanidin concentration and structural richness of flavonoids. In contrast, willows from high elevations showed greater structural richness of salicinoids and greater variation in total metabolite composition at both the intra‐ and interspecific levels. The trends in salicinoid richness and proanthocyanidin concentration were explained by elevational changes in temperature. Our results show how elevational differences in plant chemistry arise through trends in various aspects of their chemical diversity. Willows at high elevations showed reduced structural richness of metabolites involved in abiotic protection. This may reflect focused investment in metabolites with the highest ecological benefit relative to their concentration in high‐elevation willows. At the same time, they possessed greater richness of metabolites involved in biotic interactions, while variation in microhabitat preferences among high‐elevation species likely contributed to the high variation in their total metabolite pool. Read the free Plain Language Summary for this article on the Journal blog.

Understanding the phytochemical diversity of plants: Quantification, variation and ecological function

“…Studying different Salix species along elevational gradients, Volf et al (2022) found an increase in the structural diversity (MPD) of salicinoids with altitude, but a decrease for flavonoids, which may result from variation in abiotic factors. Although evidence is limited so far, these studies suggest that structural diversity can be an important aspect of the phytochemical phenotype that varies with environmental conditions and affects function.…”

“…Similar to results on evenness, Whitehead et al (2021) found that an increased structural diversity of phenolics, quantified as the mean pairwise dissimilarity (MPD) of all compounds in a mixture, increased the proportion of consumers negatively affected by the compounds. Studying different Salix species along elevational gradients, Volf et al (2022) found an increase in the structural diversity (MPD) of salicinoids with altitude, but a decrease for flavonoids, which may result from variation in abiotic factors. Although evidence is limited so far, these studies suggest that structural diversity can be an important aspect of the phytochemical phenotype that varies with environmental conditions and affects function.…”

“…Functional diversity indices, which include the disparity component of diversity (in the form of a dissimilarity matrix), have only been used in a few cases. This includes measures of mean pairwise dissimilarity (MPD; the mean of values in the compound dissimilarity matrix), which only include the disparity component (Whitehead et al 2021, Volf et al 2022), and indices such as Rao’s Q that are dependent on all three components of diversity (Bakhtiari et al 2021). A more detailed mathematical description of these indices in the context of phytochemical diversity is available in Petrén et al (2023).…”

Contrasting levels of β‐diversity and underlying phylogenetic trends indicate different paths to chemical diversity in highland and lowland willow species

“…Three of the 'lowland' species (Salix caprea, S. pentandra and S. purpurea) that typically occur in the colline and montane zones also include populations occurring in the subalpine zone. The intraspecific elevational variation in concentration or α-diversity of willow metabolites is typically smaller than interspecific differences and should not obscure the patterns explored here (Volf et al, 2022). Nonetheless, we limited our sampling of these three species to populations from the colline zone only.…”

“…They form diverse local assemblages and are broadly distributed from lowland floodplains to the alpine zone. Willow specialised metabolites mainly consist of phenolics with distinct functions, facilitating the comparison of trends in metabolites that play different roles in plant biology (Volf et al, 2015(Volf et al, , 2022. The phenolics found in willows include numerous flavonoids that are primarily involved in protecting willows against abiotic stress (Tegelberg & Julkunen-Tiitto, 2001).…”