Extreme diversification of floral volatiles within and among species of Lithophragma (Saxifragaceae)

Abstract

A major challenge in evolutionary biology is to understand how complex traits of multiple functions have diversified and codiversified across interacting lineages and geographic ranges. We evaluate intra- and interspecific variation in floral scent, which is a complex trait of documented importance for mutualistic and antagonistic interactions between plants, pollinators, and herbivores. We performed a large-scale, phylogenetically structured study of an entire plant genus (Lithophragma, Saxifragaceae), of which several species are coevolving with specialized pollinating floral parasites of the moth genus Greya (Prodoxidae). We sampled 94 Lithophragma populations distributed across all 12 recognized Lithophragma species and subspecies, and four populations of related saxifragaceous species. Our results reveal an unusually high diversity of floral volatiles among populations, species, and clades within the genus. Moreover, we found unexpectedly major changes at each of these levels in the biosynthetic pathways used by local populations in their floral scents. Finally, we detected significant, but variable, genus- and species-level patterns of ecological convergence in the floral scent signal, including an impact of the presence and absence of two pollinating Greya moth species. We propose that one potential key to understanding floral scent variation in this hypervariable genus is its geographically diverse interactions with the obligate specialized Greya moths and, in some species and sites, more generalized copollinators.

Keywords: floral parasitism; floral volatiles; geographic mosaic of coevolution; geographic variation; pollination.

Fig. 1.

(A) Average floral scent similarity (1 − Bray–Curtis distance) of Lithophragma samples from the same population, from different conspecific populations, from different species of the same Lithophragma clade, and from populations of different clades (ANOVA: F_4,32 = 65.95, P < 0.001). Different letters above bars indicate significantly different pairwise comparisons (Tukey’s honest significant difference). (B) G. politella female oviposits into the ovary and simultaneously pollinates a Lithophragma flower. Eight of the 12 Lithophragma taxa (black lines) and one outgroup taxon (H. grossulariifolia) are pollinated in this way. Within Lithophragma, two paraphyletic clades, the PAR clade and the CAM clade, are pollinated by Greya moths (phylogeny from refs. 70, 71). Dotted line indicates that L. thompsoni is a hybrid species between ancestors in the PAR and GLA clades. (C) Phylogenetic distribution of floral scent variation among populations shown as an MDS plot illustrating the 2D distance between all populations sampled.

Fig. 2.

Geographic distribution of floral scent variation for the entire floral scent bouquet at the compound group level in the PAR clade (blue line, L. parviflorum; dark green line, L. affine ssp. affine; light green line, L. affine spp. mixtum; no color, L. affine spp. trifoliatum) (A), the CAM clade (brown line, L. campanulatum; red line, L. bolanderi; orange line, L. cymbalaria; yellow line, L. heterophyllum) (B), and the non–Greya-pollinated Lithophragma species (GLA, L. glabrum; MAX, L. maximum; TEN, L. tenellum; THO, the hybrid species L. thompsoni) and outgroups (HEU, H. grossulariifolia; TEL, T. grandiflora; TIA, T. trifoliata) (C). Pies show the approximate location of each population, and colors within pies show the proportional contribution of different volatile compound groups to the population scent signal. Letters in pie sections indicate compounds that contribute more than 10% of the total scent variation in each population. Rings around pies indicate the presence of G. politella (black), G. obscura (white ring), or both G. politella and G. obscura (black and white ring).

Fig. 3.

Results of the chemical diversity (A) and nestedness analysis (B) for each of the three major Lithophragma clades (dark bars) and for individual species with more than five sampled populations (white bars). Populations of the GLA clade differed significantly from populations of the CAM and PAR clades both in number of compounds emitted and in nestedness [Tukey’s honest significant difference (HSD): P < 0.05 in both comparisons with the GLA clade], but the moth-pollinated CAM and PAR clades did not differ significantly (Tukey’s HSD: P > 0.05). Error bars in A and B denote 95% confidence intervals. (C) Number of compounds emitted and population nestedness showed a significant positive relationship (R² = 0.11, F_1,86 = 11.26, P = 0.0011).

Fig. 4.

Relationship between pairwise population-level similarity [1 − Bray–Curtis distance (dist)] and geographic distance within L. heterophyllum (light circles, populations interacting with the same combination of Greya moth pollinators; gray circles, populations with different moth pollinators) (A), L. bolanderi (light circles, same moth pollinator; gray circles, different moth pollinators) (B), L. campanulatum (C), L. cymbalaria (D), L. parviflorum (light circles, same moth pollinator; dark circles, combinations including at least one population that lack moth pollinators) (E), L. affine (light circles, same moth pollinator; gray circles, different moth pollinators) (F), L. affine spp. mixtum (G), and L. glabrum (H).