Abstract
BackgroundThe commonly invoked cost-benefit paradigm, central to most of functional biology, explains why one phenotype cannot be optimally fit in all environments; yet it is rarely tested. Trypsin proteinase inhibitors (TPIs) expression in Nicotiana attenuata is known to decrease plant fitness when plants compete with unattacked conspecifics that do not produce TPIs and also to decrease the performance of attacking herbivores.ResultsIn order to determine whether the putative benefits of TPI production outweigh its cost, we transformed N. attenuata to silence endogenous TPI production or restore it in a natural mutant that was unable to produce TPIs. We compared the lifetime seed production of N. attenuata genotypes of the same genetic background with low or no TPI to that of genotypes with high TPI levels on which M. sexta larvae were allowed to feed freely. Unattacked low TPI-producing genotypes produced more seed capsules than did plants with high TPI levels. Caterpillar attack reduced seed capsule production in all genotypes and reversed the pattern of seed capsule production among genotypes. M. sexta larvae attacking genotypes with high TPI activity consumed more TPI, less protein, and move later to the young leaves. Larval masses were negatively correlated (R2 = 0.56) with seed capsule production per plant.ConclusionsOur results demonstrate that the fitness benefits of TPI production outweigh their costs in greenhouse conditions, when plants are attacked and that despite the ongoing evolutionary interactions between plant and herbivore, TPI-mediated decreases in M. sexta performance translates into a fitness benefit for the plant.
Highlights
The commonly invoked cost-benefit paradigm, central to most of functional biology, explains why one phenotype cannot be optimally fit in all environments; yet it is rarely tested
Spatial and temporal distribution of plant Trypsin proteinase inhibitors (TPIs)/protein contents In order to determine the effect of caterpillar attack on TPI activity, measurements were made from all rosette and stem leaves before, and 4 and 11 d after larvae started to feed on S1 leaves (Fig. 1) from transformed (AS, anti-sense orientation (AS), and S++) and untransformed (WT and A) genotypes (Fig. 2 and Fig. 1-4/Appendix 1 [see Additional file 1])
Constitutive TPI levels in all genotypes on day 0 were higher in rosette leaves than in stem leaves (F1,70-AS – = 217.13; P
Summary
The commonly invoked cost-benefit paradigm, central to most of functional biology, explains why one phenotype cannot be optimally fit in all environments; yet it is rarely tested. The cost-benefit paradigm is central to functional biology and to ecological and evolutionary theory because fitness costs and benefits associated with a trait determine its equilibrium value in a population. Herbivores can reduce seed production and other correlates of plant fitness, and this reduction can result in natural selection for either constitutively expressed or inducible plant defenses [8,9,10]. Defenses might benefit plants in the presence of herbivores, plant resistance to herbivores can be costly in the absence of enemies, and inducible expression of resistance traits allow plants to forgo or, to pay the potential fitness cost of resistance traits when they are needed [3,5,11,12,13,14]
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