A below-ground herbivore shapes root defensive chemistry in natural plant populations

Abstract

Plants display extensive intraspecific variation in secondary metabolites. However, the selective forces shaping this diversity remain often unknown, especially below ground. Using Taraxacum officinale and its major native insect root herbivore Melolontha melolontha, we tested whether below-ground herbivores drive intraspecific variation in root secondary metabolites. We found that high M. melolontha infestation levels over recent decades are associated with high concentrations of major root latex secondary metabolites across 21 central European T. officinale field populations. By cultivating offspring of these populations, we show that both heritable variation and phenotypic plasticity contribute to the observed differences. Furthermore, we demonstrate that the production of the sesquiterpene lactone taraxinic acid b-D-glucopyranosyl ester (TA-G) is costly in the absence, but beneficial in the presence of M. melolontha, resulting in divergent selection of TA-G. Our results highlight the role of soil-dwelling insects for the evolution of plant defences in nature. BackgroundHeritable intraspecific variation is a common feature of many biological traits. Genetic variation results from heterogeneous selection pressures in relation to genetic architecture, population substructures and gene flow [1 -4]. In plants, local differences in both abiotic and biotic factors may drive trait evolution [5]. Insect herbivores, the most abundant and diverse plant consumers, have long been suspected to play an important role in this context [6]. Recent studies demonstrate that herbivore abundance can covary with the expression of plant defence metabolites [7], that the exclusion of phytophagous insects can lead to a relaxation of defences within a few generations [8] and that defence genes are under differential selection across environments [9,10]. Together, these studies show that the temporal and spatial variation in above-ground herbivore communities can shape plant defensive chemistry.In contrast with the ecological and evolutionary dynamics of above-ground plant-herbivore interactions, below-ground interactions have received little attention, despite the importance of roots for plant fitness and the high concentrations of secondary metabolites in below-ground organs [11][12][13][14]. The rhizosphere differs from the phyllosphere in both biotic and abiotic conditions [15], and the selective forces shaping variation in secondary metabolites may therefore differ between the two environments. The evolution of root secondary metabolites may for instance be driven by herbivores [11,12,16], pathogens [17] and symbionts [18], as well as nutrient availability [19], salt, drought and cold stress [20]. By comparing one mainland and two island populations, Watts et al. [21] showed that geographical isolation, including the escape from pocket gophers (Geomyidae), resulted in the evolutionary decline of root alkaloid concentrations of the host plant Eschscholzia californica (Papaveraceae). The specific potential of root herbivores to shap...

Insect herbivory and plant adaptation in an early successional community*

“…In dandelion roots, TA‐G concentration is likely under positive selection by belowground feeding generalist insects (Huber et al. ,b). Dandelion populations exposed to severe belowground herbivory over several decades had higher TA‐G concentration in their root latex compared to lightly infested populations in the field; both phenotypic plasticity and genotypic differentiation contributed to this differentiation.…”

“…Although total PIE concentration in root latex was higher in dandelion populations subject to long‐term root herbivory compared to controls, this pattern was likely shaped predominantly by phenotypic plasticity (Huber et al. ). These results compared to the current study highlight that the evolution of plant defense chemistry can be distinct above and belowground, and the extent of pleiotropy between these plant compartments awaits further study.…”

“…Nonetheless, the induction of PIEs in the leaves by above ground herbivores contrasts with the reduction of these compounds in root latex upon below ground herbivore attack (Huber et al. ,b). Differences in the genotype composition, herbivore identity, and feeding intensity may account for the divergent responses.…”

“…We also searched for root feeding herbivores, which have been shown to be important in the evolution of dandelion defense in Europe (Huber et al. , b), but did not find any.…”

“…We focused on two classes of plant defense, sesquiterpene lactones and phenolic inositol esters, which were recently shown to be important in the defense of dandelion against herbivory (Huber et al. , ,b). Thus, the current study investigates the roles of herbivory and succession in shaping the genetic structure of dandelion populations and the evolutionary ecology of their defense chemistry.…”