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Constitutive and herbivore-induced plant defenses regulate herbivore population growth.

1.Herbivore-induced plant defenses regulated by the phytohormones jasmonic acid and salicylic acid are predicted to influence herbivore population dynamics, in part because they can operate in a density-dependent manner. While there is ample evidence that herbivore-induced plant responses affect individual performance and growth of herbivores, whether they scale-up to regulate herbivore population dynamics is still unclear. 2.We evaluated the consequences of variation in plant defenses and herbivore density on herbivore development, reproduction and density-dependent population growth. We investigated potential mechanisms affecting the strength of herbivore density-dependent processes by manipulating jasmonate expression, quantifying plant defensive traits (phytohormones jasmonic acid and salicylic acid and serine proteinase inhibitors) and adding aphids (Macrosiphum euphorbiae) at different densities to plants to simulate different initial population density and herbivore load. We manipulated jasmonate defenses by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate-dependent defenses. Jasmonate-insensitive plants cannot induce the defenses regulated by the jasmonic acid pathway, while jasmonate-overexpressing plants constitutively express jasmonate-dependent defenses. 3.We found that jasmonate defenses provided resistance against aphids and influenced density-dependent processes. Jasmonate-overexpressing plants reduced aphid reproduction, prolonged developmental time, dampened aphid populations across all aphid densities, and caused density-independent aphid population growth. Jasmonate-overexpressing plants showed high JA-dependent constitutive levels of resistance and were unable to activate the salicylic acid pathway in response to aphid feeding. In contrast, jasmonate-insensitive plants increased aphid reproduction, shortened developmental time, reduced population growth only at high initial densities, and promoted strong negative density-dependent population growth. Aphid feeding on jasmonate-insensitive plants did not induce jasmonate-dependent defenses, but induced the salicylic acid pathway in a density-dependent manner, which resulted in negative density-dependent aphid population growth. 4.Aphid feeding on jasmonate-insensitive and overexpressing plants differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones jasmonic acid and salicylic acid. By muting or enhancing jasmonate-mediated responses and quantifying salicylic acid phytohormone induction, we demonstrated that plant defenses are a key factor driving not only the performance, but also the density dependence processes and population growth of herbivores. This article is protected by copyright. All rights reserved.

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