Dataset Information

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 fast-growing 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.

SUBMITTER: Cope OL

PROVIDER: S-EPMC8449370 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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

Cope Olivia L OL Keefover-Ring Ken K Kruger Eric L EL Lindroth Richard L RL

Proceedings of the National Academy of Sciences of the United States of America 20210901 37

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 def ...[more]

PMID: 34507992

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Project description:Background and aimsIntraspecific variation in foundation species of forest ecosystems can shape community and ecosystem properties, particularly when that variation has a genetic basis. Traits mediating interactions with other species are predicted by simple allocation models to follow ontogenetic patterns that are rarely studied in trees. The aim of this research was to identify the roles of genotype, ontogeny and genotypic trade-offs shaping growth, defence and reproduction in aspen.MethodsWe established a common garden replicating >500 aspen genets in Wisconsin, USA. Trees were measured through the juvenile period into the onset of reproduction, for growth, defence chemistry (phenolic glycosides and condensed tannins), nitrogen, extrafloral nectaries, leaf morphology (specific leaf area), flower production and foliar herbivory and disease. We also assayed the TOZ19 sex marker and heterozygosity at ten microsatellite loci.Key resultsWe found high levels of genotypic variation for all traits, and high heritabilities for both the traits and their ontogenetic trajectories. Ontogeny strongly shaped intraspecific variation, and trade-offs among growth, defence and reproduction supported some predictions while contradicting others. Both direct resistance (chemical defence) and indirect defence (extrafloral nectaries) declined during the juvenile stage, prior to the onset of reproduction. Reproduction was higher in trees that were larger, male and had higher individual heterozygosity. Growth was diminished by genotypic allocation to both direct and indirect defence as well as to reproduction, but we found no evidence of trade-offs between defence and reproduction.ConclusionsKey traits affecting the ecological communities of aspen have high levels of genotypic variation and heritability, strong patterns of ontogeny and clear trade-offs among growth, defence and reproduction. The architecture of aspen's community genetics - its ontogeny, trade-offs and especially its great variability - is shaped by both its broad range and the diverse community of associates, and in turn further fosters that diversity.

Project description:Long-term overgrazing (OG) is one of the key drivers of global grassland degradation with severe loss of productivity and ecosystem functions, which may result in stress memory such as smaller stature of grassland plants. However, how the OG-induced stress memory could be regulated by phytohormones is unknown. In this study, we investigated the changes of four phytohormones of cloned offspring of Leymus chinensis that were developed from no-grazing (NG) plants and OG plants with a grazing history of 30 years. The concentrations of auxin (IAA) and gibberellic acid (GA) in OG plant leaves were 45% and 20% lower than control, respectively. Meanwhile, the level of abscisic acid (ABA) in OG leaves nearly doubled compared with that in NG leaves. The situation was quite similar in roots. Unexpectedly, no significant changes in the jasmonic acid (JA) level were observed between OG and NG plants. The changes in gene expression patterns between OG and NG plants were also investigated by transcriptomic analysis. In total, 302 differentially expressed genes (DEGs) were identified between OG and NG plants, which were mainly classified into the functions of synthesis, receptor, and signal transduction processes of phytohormones. The expression of 24 key genes related to the biosynthesis and signal transduction of IAA and GA was downregulated in OG plants. Among them, OASA1 and AO1 (regulating the biosynthesis of IAA and ABA, respectively) were reduced significantly by 88 and 92%, respectively. In addition, the content of secondary metabolites related to plant defense such as flavonoids and phenols was also increased in leaves. Taken together, the decrease of positive plant growth-related hormones (IAA and GA) together with the increase of plant stress-related hormones or factors (ABA, flavonoids, and phenols) induced the growth-defense trade-offs for L. chinensis adaptation to long-term OG stress. The findings reported in this study shed new light on the mechanism of plant-animal interaction in the grassland ecosystem and provide a deeper insight into optimizing grazing management and sustainable utilization of grassland.

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

Publications

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

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