Growth-defense trade-offs shape population genetic composition in an iconic forest tree species

Abstract

All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a pivotal conflict occurs between allocation to growth, which accelerates resource acquisition, and to defense, which protects existing tissue against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of plant evolutionary ecology is that context-dependence of these trade-offs contributes to the maintenance of intraspecific variation in defense [Züst and Agrawal, Annu. Rev. Plant Biol., 68, 513-534 (2017)]. This prediction has rarely been tested, however, and the evolutionary consequences of growth- defense trade-offs in different environments are poorly understood, especially in long-lived species [Cipollini et al., Annual Plant Reviews (Wiley, 2014), pp. 263-307]. Here we show that intraspecific trait trade-offs, even when fixed across divergent environments, interact with competition to drive natural selection of tree genotypes corresponding to their growth-defense phenotypes. Our results show that a functional trait trade-off, when coupled with environmental variation, causes real-time divergence in the genetic architecture of tree populations in an experimental setting. Specifically, competitive selection for faster growth resulted in dominance by fastgrowing tree genotypes that were poorly defended against natural enemies. This outcome is a signature example of eco-evolutionary dynamics: Competitive interactions affected microevolutionary trajectories on a timescale relevant to subsequent ecological interactions [Brunner et al., Funct. Ecol. 33, 7-12 (2019)]. Eco-evolutionary drivers of tree growth and defense are thus critical to stand-level trait variation, which structures communities and ecosystems over expansive spatiotemporal scales.