skip to main content


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

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 [Cipolliniet 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 [Brunneret 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.

 
more » « less
NSF-PAR ID:
10305838
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
118
Issue:
37
ISSN:
0027-8424
Page Range / eLocation ID:
Article No. e2103162118
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Interactions between neighboring plants are critical for biodiversity maintenance in plant populations and communities. Intraspecific trait variation and genome duplication are common in plant species and can drive eco‐evolutionary dynamics through genotype‐mediated plant–plant interactions. However, few studies have examined how species‐wide intraspecific variation may alter interactions between neighboring plants. We investigate how subspecies and ploidy variation in a genetically diverse species, big sagebrush (Artemisia tridentata), can alter the demographic outcomes of plant interactions. Using a replicated, long‐term common garden experiment that represents range‐wide diversity ofA. tridentata, we ask how intraspecific variation, environment, and stand age mediate neighbor effects on plant growth and survival. Spatially explicit models revealed that ploidy variation and subspecies identity can mediate plant–plant interactions but that the effect size varied in time and across experimental sites. We found that demographic impacts of neighbor effects were strongest during early stages of stand development and in sites with greater growth rates. Within subspecies, tetraploid populations showed greater tolerance to neighbor crowding compared to their diploid variants. Our findings provide evidence that intraspecific variation related to genome size and subspecies identity impacts spatial demography in a genetically diverse plant species. Accounting for intraspecific variation in studies of conspecific density dependence will improve our understanding of how local populations will respond to novel genotypes and biotic interaction regimes. As introduction of novel genotypes into local populations becomes more common, quantifying demographic processes in genetically diverse populations will help predict long‐term consequences of plant–plant interactions.

     
    more » « less
  2. Abstract

    Local adaptation is common in plants, yet characterization of its underlying genetic basis is rare in herbaceous perennials. Moreover, while many plant species exhibit intraspecific chemical defence polymorphisms, their importance for local adaptation remains poorly understood. We examined the genetic architecture of local adaptation in a perennial, obligately‐outcrossing herbaceous legume, white clover (Trifolium repens). This widespread species displays a well‐studied chemical defence polymorphism for cyanogenesis (HCN release following tissue damage) and has evolved climate‐associated cyanogenesis clines throughout its range. Two biparental F2 mapping populations, derived from three parents collected in environments spanning the U.S. latitudinal species range (Duluth, MN, St. Louis, MO and Gainesville, FL), were grown in triplicate for two years in reciprocal common garden experiments in the parental environments (6,012 total plants). Vegetative growth and reproductive fitness traits displayed trade‐offs across reciprocal environments, indicating local adaptation. Genetic mapping of fitness traits revealed a genetic architecture characterized by allelic trade‐offs between environments, with 100% and 80% of fitness QTL in the two mapping populations showing significant QTL×E interactions, consistent with antagonistic pleiotropy. Across the genome there were three hotspots of QTL colocalization. Unexpectedly, we found little evidence that the cyanogenesis polymorphism contributes to local adaptation. Instead, divergent life history strategies in reciprocal environments were major fitness determinants: selection favoured early investment in flowering at the cost of multiyear survival in the southernmost site versus delayed flowering and multiyear persistence in the northern environments. Our findings demonstrate that multilocus genetic trade‐offs contribute to contrasting life history characteristics that allow for local adaptation in this outcrossing herbaceous perennial.

     
    more » « less
  3. Summary

    Intraspecific variation in functional traits may mediate tree species' drought resistance, yet whether trait variation is due to genotype (G), environment (E), or G×E interactions remains unknown. Understanding the drivers of intraspecific trait variation and whether variation mediates drought response can improve predictions of species' response to future drought.

    Using populations of quaking aspen spanning a climate gradient, we investigated intraspecific variation in functional traits in the field as well as the influence of G and E among propagules in a common garden. We also tested for trait‐mediated trade‐offs in growth and drought stress tolerance.

    We observed intraspecific trait variation among the populations, yet this variation did not necessarily translate to higher drought stress tolerance in hotter/drier populations. Additionally, plasticity in the common garden was low, especially in propagules derived from the hottest/driest population. We found no growth–drought stress tolerance trade‐offs and few traits exhibited significant relationships with mortality in the natural populations, suggesting that intraspecific trait variation among the traits measured did not strongly mediate responses to drought stress.

    Our results highlight the limits of trait‐mediated responses to drought stress and the complex G×E interactions that may underlie drought stress tolerance variation in forests in dry environments.

     
    more » « less
  4. Abstract

    Understanding the mechanisms that promote the coexistence of hundreds of species over small areas in tropical forest remains a challenge. Many tropical tree species are presumed to be functionally equivalent shade tolerant species but exist on a continuum of performance trade‐offs between survival in shade and the ability to quickly grow in sunlight. These trade‐offs can promote coexistence by reducing fitness differences.

    Variation in plant functional traits related to resource acquisition is thought to predict variation in performance among species, perhaps explaining community assembly across habitats with gradients in resource availability. Many studies have found low predictive power, however, when linking trait measurements to species demographic rates.

    Seedlings face different challenges recruiting on the forest floor and may exhibit different traits and/or performance trade‐offs than older individuals face in the eventual adult niche. Seed mass is the typical proxy for seedling success, but species also differ in cotyledon strategy (reserve vs. photosynthetic) or other leaf, stem and root traits. These can cause species with the same average seed mass to have divergent performance in the same habitat.

    We combined long‐term studies of seedling dynamics with functional trait data collected at a standard life‐history stage in three diverse neotropical forests to ask whether variation in coordinated suites of traits predicts variation among species in demographic performance.

    Across hundreds of species in Ecuador, Panama and Puerto Rico, we found seedlings displayed correlated suites of leaf, stem, and root traits, which strongly correlated with seed mass and cotyledon strategy. Variation among species in seedling functional traits, seed mass, and cotyledon strategy were strong predictors of trade‐offs in seedling growth and survival. These results underscore the importance of matching the ontogenetic stage of the trait measurement to the stage of demographic dynamics.

    Our findings highlight the importance of cotyledon strategy in addition to seed mass as a key component of seed and seedling biology in tropical forests because of the contribution of carbon reserves in storage cotyledons to reducing mortality rates and explaining the growth‐survival trade‐off among species.

    Synthesis: With strikingly consistent patterns across three tropical forests, we find strong evidence for the promise of functional traits to provide mechanistic links between seedling form and demographic performance.

     
    more » « less
  5. Abstract

    Spatiotemporal variation in herbivory is a major driver of intraspecific variation in plant defense. Comparatively little is known, however, about how changes in herbivory regime affect the balance of constitutive and induced resistance, which are often considered alternative defensive strategies. Here, we investigated how nearly a decade of insect herbivore suppression affected constitutive and induced resistance in horsenettle (Solanum carolinense), a widespread herbaceous perennial. We allowed replicated horsenettle populations to respond to the presence or absence of herbivores by applying insecticide to all plants in half of 16 field plots. Horsenettle density rapidly increased in response to insecticide treatment, and this effect persisted for at least 4 years after the cessation of herbivore suppression. We subsequently grew half‐sibling families from seeds collected during and shortly after insecticide treatment in a common garden and found strong effects of insect suppression on induced resistance. Feeding trials in field mesocosms with false Colorado potato beetles (Leptinotarsa juncta), a common specialist herbivore, revealed that multiyear herbivore suppression drove rapid attenuation of induced resistance: offspring of plants from insect‐suppression plots exhibited a near‐complete loss of induced resistance to beetles, whereas those from control plots incurred ~70% less damage after experimental induction. Plants from insect‐suppression plots also had ~40% greater constitutive resistance compared with those from control plots, although this difference was not statistically significant. We nonetheless detected a strong trade‐off between constitutive and induced resistance across families. In contrast, the constitutive expression of trypsin inhibitors (TI), an important chemical defense trait in horsenettle, was reduced by 20% in the offspring of plants from insect‐suppression plots relative to those from control plots. However, TIs were induced to an equal extent whether or not insect herbivores had been historically suppressed. Although several defense and performance traits (prickle density, TI concentration, resistance against false Colorado potato beetles and flea beetles, biomass, and seed mass) varied markedly across families, no traits exhibited significant pairwise correlations. Overall, our results indicate that, whereas the divergent responses of multiple defense traits to insect suppression led to comparatively small changes in overall constitutive resistance, they significantly reduced induced resistance against false Colorado potato beetle.

     
    more » « less