Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability

1. Production of antiherbivore chemical defences is generally assumed to be costly in terms of fitness, although some studies have failed to detect such costs. A convincing explanation is that the expression of fitness costs depends on environmental conditions such as nutrient availability. 2. We performed a greenhouse experiment with 33 half-sib families in order to study the phenotypic plasticity of constitutive and methyl jasmonate-induced chemical defences to soil phosphorus (P) availability, the existence of genetic trade-offs (costs) between growth and the production of those defences and the extent to which P availability may modulate the expression of those costs. 3. We measured some proxies of vegetative fitness (primary growth, secondary growth and total biomass), plant reserves (soluble sugars and starch) and the concentration of quantitative chemical defences (diterpene content in the stem, total polyphenolics and condensed tannins in the needles). 4. Phosphorus availability had a considerable effect, both on the allocation of resources to constitutive and induced defences and on the expression of vegetative costs associated with those chemical defences. Constitutive investment in chemical defences was greater under P-limited conditions for all studied traits. Inducibility of foliar phenolic compounds was greater under P-limited conditions, and it was strongly constrained under high P availability. Availability of P did not affect the inducibility of stem diterpenes. 5. All defensive traits showed significant genetic variation, with different levels of genetic control in constitutive and induced modes, and genetic variation in their inducibility. We found significant negative genetic correlations (i.e. trade-offs) between growth and defensive investment, but costs of chemical defences emerged only in P-limited conditions. Vegetative costs of constitutive defences were detected for stem diterpenes but not for needle phenolics, while costs of induced defences were found for leaf phenolics but not for stem diterpenes. 6. Synthesis. Our results indicate that P availability controls the production of chemical defences in this pine species, influencing the resource allocation to constitutive defences, the inducibility of those defences and the emergence of related vegetative costs. Phosphorus availability thus appears as a major driver in the evolution of pine resistance to insects and a potential factor in maintaining genetic variation in defences.This research was supported by the grants RTA07-100, PSE310000, AGL2010-18724 and CSIC-200840I153 from the Spanish MCIN. L.S. and X.M. received financial support from DOC-INIA and PREDOC-INIA grant programs respectively