Growth-defense tradeoffs shape the genetic makeup of the population of an iconic forest species
Genetic diversity is essential for ecological resilience and is maintained when different traits are advantageous in different environments. Traits are not, however, entirely independent: when trade-offs occur, selection on one trait may act indirectly on another. Here, we examine how environment-mediated selection for growth interacts with a trade-off between growth and herbivore defense in experimental aspen stands. We show that even an environmentally fixed trait compromise can lead to real-time divergence in the genetic makeup of the population between environments. The underlying growth-defense trade-off led to an eco-evolutionary dynamic in which highly competitive environments were selected for fast-growing trees and therefore ultimately selected against herbivore resistance. This discovery reveals how patterns of genetic covariation, associated with environmental variation, can link ecological and evolutionary processes.
All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a crucial conflict occurs between allocation to growth, which accelerates the acquisition of resources, and defense, which protects existing tissues against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of evolutionary plant ecology is that context dependence of these compromises contributes to the maintenance of intraspecific variation in defense. [Züst and Agrawal, Annu. Rev. Plant Biol., 68, 513–534 (2017)]. However, this prediction has rarely been tested and the evolutionary consequences of growth-defense trade-offs in different environments are poorly understood, particularly in long-lived species. [Cipollini et al., Annual Plant Reviews (Wiley, 2014), pp. 263–307]. Here, we show that intraspecific trait compromises, even when fixed in divergent environments, interact with competition to lead to the natural selection of tree genotypes corresponding to their growth-defense phenotypes. Our results show that a compromise of functional traits, when associated 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 the dominance of fast growing tree genotypes that were poorly defended against natural enemies. This result is an emblematic example of eco-evolutionary dynamics: competitive interactions have affected micro-evolutionary trajectories on a time scale relevant for subsequent ecological interactions. [Brunner et al., Funct. Ecol. 33, 7–12 (2019)]. Eco-evolutionary drivers of tree growth and defense are therefore central to the variation in stand-level traits, which structures communities and ecosystems over vast spatiotemporal scales.
Author contributions: research designed by KK-R., ELK and RLL; OLC, KK-R., ELK and RLL searched; Data analyzed by OLC; and OLC, KK-R., ELK and RLL wrote the article.
The authors declare no competing interests.
This article is a direct PNAS submission.
This article contains additional information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2103162118/-/DCSupplemental.
The dataset associated with the current study is available in the Dryad data repository (DOI: 10.5061 / dryad.x95x69phb) (58).