Pollen sterols are associated with phylogeny and environment but not with pollinator guilds

Abstract

Phytosterols are primary plant metabolites that have fundamental structural and regulatory functions. They are also essential nutrients for phytophagous insects, including pollinators, that cannot synthesize sterols. Despite the well-described composition and diversity in vegetative plant tissues, few studies have examined phytosterol diversity in pollen. We quantified 25 pollen phytosterols in 122 plant species (105 genera, 51 families) to determine their composition and diversity across plant taxa. We searched literature and databases for plant phylogeny, environmental conditions, and pollinator guilds of the species to examine the relationships with pollen sterols. 24-methylenecholesterol, sitosterol and isofucosterol were the most common and abundant pollen sterols. We found phylogenetic clustering of twelve individual sterols, total sterol content and sterol diversity, and of sterol groupings that reflect their underlying biosynthesis pathway (C-24 alkylation, ring B desaturation). Plants originating in tropical-like climates (higher mean annual temperature, lower temperature seasonality, higher precipitation in wettest quarter) were more likely to record higher pollen sterol content. However, pollen sterol composition and content showed no clear relationship with pollinator guilds. Our study is the first to show that pollen sterol diversity is phylogenetically clustered and that pollen sterol content may adapt to environmental conditions.

Keywords: chemical ecology; chemotaxonomy; environmental factors; phylogeny; phytosterol diversity; plant-insect interactions; pollen nutrients; pollinator guild.

Fig. 1

Chemical structure of 24‐methylenecholesterol as an illustration of phytosterols, showing (a) carbon numbering (b) different substitutions in ring B, and (c) different substitutions at C‐24.

Fig. 2

Pollen sterol profiles of plant species. Phylogenetic relationships are given on the left; bold numbers indicate families. Relative contributions of individual sterols to each species’ total sterol content are given in the centre; commonness (proportion of plants containing an individual sterol) and relative abundance (average proportion of individual sterol in each species) are given at the bottom. Deeper reds indicate values closer to 1. Shannon diversity index (H), C‐24 groups (C0, C1, C2), Δ groups (D0, D5, D7, D8), and total sterol content are given on the right. Circle size represents sums of relative sterol contents in the respective groups (0 to 1), and log of µg mg^–1 pollen for total sterol content. Sterol names and groups are coloured in the same fashion as illustrated in Fig. 1. Families: 1, Pinaceae; 2, Nymphaeaceae; 3, Colchicaceae; 4, Cannaceae; 5, Strelitziaceae; 6, Iridaceae; 7, Asphodelaceae; 8, Asparagaceae; 9, Amaryllidaceae; 10, Ranunculaceae; 11, Papaveraceae; 12, Paeoniaceae; 13, Geraniaceae; 14, Myrtaceae; 15, Onagraceae; 16, Cistaceae; 17, Malvaceae; 18, Oxalidaceae; 19, Salicaceae; 20, Linaceae; 21, Euphorbiaceae; 22, Fagaceae; 23, Cucurbitaceae; 24, Rosaceae; 25, Fabaceae; 26, Droseraceae; 27, Caryophyllaceae; 28, Nyctaginaceae; 29, Cactaceae; 30, Hydrangeaceae; 31, Polemoniaceae; 32, Theaceae; 33, Ericaceae; 34, Primulaceae; 35, Araliaceae; 36, Apiaceae; 37, Adoxaceae; 38, Caprifoliaceae; 39, Campanulaceae; 40, Menyanthaceae; 41, Asteraceae; 42, Apocynaceae; 43, Convolvulaceae; 44, Solanaceae; 45, Boraginaceae; 46, Gesneriaceae; 47, Scrophulariaceae; 48, Plantaginaceae; 49, Bignoniaceae; 50, Phrymaceae; 51, Lamiaceae.

Fig. 3

Hypothetical biosynthetic pathways of phytosterols identified in this study (pathways based on Benveniste, 2004). Details of C‐24 and delta groups see Fig. 1.

Fig. 4

Correlation plots of phylogenetically independent contrasts (PICs) of positions on the environmental principal component axes (PC1–PC3) and environmental niche breadth against PICs of total pollen sterol amounts (top row) and sterol profile Shannon diversity indices (H, bottom row). Blue dashed lines indicate regression lines of linear models (with intercept set to zero); r ² and P‐values for linear models have been inserted into their respective plots. For PC loadings from each environmental variable see Supporting Information Table S3.

Fig. 5

2D‐non‐metric multidimensional scaling (NMDS) plots of sterol profiles for plants (a) with different pollinator guilds, and (b) with/without pollen as bee reward. Distances correspond to sterol profile dissimilarity (Bray–Curtis distances). Stress of NMDS solution: 0.202.