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

Abstract

Summary1. 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.

Additive genetic variation in resistance traits of an exotic pine species: little evidence for constraints on evolution of resistance against native herbivores

“…Although the emergence of this type of cost-related trade-offs has been shown to be context dependent (Sampedro et al, 2011a), our results suggest no constraints for the independent evolution of these two functions in the studied population of this exotic pine species. The EICA hypothesis, one of the central tenets of invasion biology theory, predicts that exotic plant species suffer less damage by herbivores in their introduced ranges and they might thus reallocate fewer resources to defence and more to growth and reproduction.…”

“…The EICA hypothesis, one of the central tenets of invasion biology theory, predicts that exotic plant species suffer less damage by herbivores in their introduced ranges and they might thus reallocate fewer resources to defence and more to growth and reproduction. In addition to the differential herbivore pressures, this outcome arises because plant defence/resistance traits are energetically expensive to produce and maintain, and therefore it is commonly assumed that resistance and fitness traits trade-off with each other (Messina et al, 2002;Donaldson et al, 2006;Sampedro et al, 2011a). The existence of such trade-offs between defence and fitness traits may explain why exotic plant species are usually more vigorous in non-indigenous habitats (usually with reduced load of enemies) than in their natural range.…”

“…Ltd, Maidstone, Kent, UK) into new preweighed test tubes, and the entire extraction step was then repeated again. The solvent in the tubes was evaporated to dryness and the mass of the non-volatile resin residue was determined at the nearest 0.0001 g. This gravimetric determination of non-volatile resin was highly correlated with the concentration of the diterpenoid fraction (r ¼ 0.9214; P ¼ 0.00002), as quantified by gas chromatography in previous trials (Sampedro et al, 2011a).…”

“…Total phenolic content was determined colorimetrically by the Folin-Ciocalteu method in a Biorad 650 microplate reader (Bio-Rad Laboratories Inc., Philadelphia, PA, USA) at 740 nm, using tannic acid as standard, and referred to the vegetal tissue in a dried weight (d.w.) basis. Concentration of non-volatile resin in the stem was estimated gravimetrically (Sampedro et al, 2011a) and expressed as mg of non-volatile resin g À1 stem d.w. Subsequently, about 5 g fresh weight of stem material was transferred into preweighed borosilicate test tubes, resin was extracted with 3 ml of hexane (15 min at 20 1C in an ultrasonic bath and then for 24 h at room temperature), the extract was filtered (Whatman GFF, Whatman Int.…”

“…Assuming that the production of plant defences is costly in terms of growth and fitness, current theories on the evolution of plant resistance predict the existence of evolutionary trade-offs (negative genetic correlations) between resistance and fitness traits (Messina et al, 2002;Donaldson et al, 2006;Sampedro et al, 2011a), and between different resistance traits (reviewed by Koricheva et al (2004)). The existence of these trade-offs may severely constrain the invasion success of plant populations in non-indigenous habitats, as trade-offs limit the simultaneous change of negatively correlated traits (Orians and Ward, 2010).…”