Knowledge of the manner in which genetic variation within a tree species affects associated communities and ecosystem processes across its entire range is important for understanding how geographic mosaics of genetic interactions might develop and support different communities. While numerous studies have investigated the community and ecosystem consequences of genetic variation at the hybrid cross type or genotype level within a species, none has investigated the community‐level effects of intraspecific genetic variation across the geographic range of a widespread species. This is the scale at which geographic mosaics of coevolution are hypothesized to exist. Studies at this level are particularly important for foundation tree species, which typically support numerous microbial, fungal, plant, and animal communities. We studied genetic variation across eight geographical races of the forest tree Eucalyptus globulus representing its natural distribution across southeastern Australia. The study was conducted in a 15‐year‐old common garden trial based on families derived from single‐tree open‐pollinated seed collections from the wild. Neutral molecular genetic variation within E. globulus was also assessed and compared with genetic divergence in the phenotypic and community traits. Three major findings emerged. First, we found significant genetically based, hierarchical variation in associated communities corresponding to geographical races of E. globulus and families within races. Second, divergence in foliar communities at the racial level was associated with genetically based divergence in specific leaf morphological and chemical traits that have known defensive functions. Third, significant positive correlations between canopy community dissimilarity and both neutral molecular genetic and leaf quantitative genetic dissimilarity at the race level supported a genetic similarity rule. Our results argue that genetic variation within foundation tree species has the potential to be a significant driver of the geographical mosaics of variation typical of forest communities, which could have important ecological and evolutionary implications.

Summary: In the field of plant–herbivore interactions a major focus of research is the importance of herbivores as selective agents on the evolution of plant resistance. Evidence to support the role of herbivores as selective agents must demonstrate that the intraspecific variation in plant resistance, and the variation in the plant resistive trait, are under genetic control. Predominantly, research in this field has concentrated on plant–insect systems, with much less emphasis on plant–mammal interactions. In a common Eucalyptus species, Eucalyptus globulus (Labill.), variation in resistance to a mammalian herbivore, Trichosurus vulpecula (Kerr, 1792), is under genetic control. In this paper, plants of known genetic stock grown in a common‐environment field trial were used to investigate the plant characteristic responsible for resistance of E. globulus to T. vulpecula and to determine if there was a genetic basis to variation in the defensive trait. The results demonstrate that a formylated phloroglucinol compound, sideroxylonal, is the dominant plant secondary metabolite that determined intake of E. globulus juvenile coppiced foliage by T. vulpecula, and that this metabolite is under significant genetic control. These results are discussed in the context of the possible role T. vulpecula may play as a selective agent on the evolution of resistance in E. globulus.

A central issue in our understanding of the evolution of the diversity of plant secondary metabolites (PSMs) is whether or not compounds are functional, conferring an advantage to the plant, or non-functional. We examine the hypothesis that the diversity of monoterpene PSMs within a plant species (Scots pine Pinus sylvestris ) may be explained by different compounds acting as defences against high-impact herbivores operating at different life stages. We also hypothesize that pairwise coevolution, with uncorrelated interactions, is more likely to result in greater PSM diversity, than diffuse coevolution. We tested whether up to 13 different monoterpenes in Scots pine were inhibitory to herbivory by slugs ( Arion ater ), bank voles ( Clethrionomys glareolus ), red deer ( Cervus elaphus ) and capercaillie ( Tetrao urogallus) , each of which attack trees at a different life stage. Plants containing more α-pinene were avoided by both slugs and capercaillie, which may act as reinforcing selective agents for this dominant defensive compound. Herbivory by red deer and capercaillie were, respectively, weakly negatively associated with δ ³ -carene, and strongly negatively correlated with the minor compound β-ocimene. Three of the four herbivores are probably contributory selective agents on some of the terpenes, and thus maintain some, but by no means all, of the phytochemical diversity in the species. The correlated defensive function of α-pinene against slugs and capercaillie is consistent with diffuse coevolutionary processes.