skip to main content

Explore Research Products in the NSF-PAR

Title: Unraveling the roles of genotype and environment in the expression of plant defense phenotypes
Abstract

Phenotypic variability results from interactions between genotype and environment and is a major driver of ecological and evolutionary interactions. Measuring the relative contributions of genetic variation, the environment, and their interaction to phenotypic variation remains a fundamental goal of evolutionary ecology.

In this study, we assess the question: How do genetic variation and local environmental conditions interact to influence phenotype within a single population? We explored this question using seed from a single population of common milkweed,Asclepias syriaca, in northern Michigan. We first measured resistance and resistance traits of 14 maternal lines in two common garden experiments (field and greenhouse) to detect genetic variation within the population. We carried out a reciprocal transplant experiment with three of these maternal lines to assess effects of local environment on phenotype. Finally, we compared the phenotypic traits measured in our experiments with the phenotypic traits of the naturally growing maternal genets to be able to compare relative effect of genetic and environmental variation on naturally occurring phenotypic variation. We measured defoliation levels, arthropod abundances, foliar cardenolide concentrations, foliar latex exudation, foliar carbon and nitrogen concentrations, and plant growth.

We found a striking lack of correlation in trait expression of the maternal lines between the common gardens, or between the common gardens and the naturally growing maternal genets, suggesting that environment plays a larger role in phenotypic trait variation of this population. We found evidence of significant genotype‐by‐environment interactions for all traits except foliar concentrations of nitrogen and cardenolide. Milkweed resistance to chewing herbivores was associated more strongly with the growing environment. We observed no variation in foliar cardenolide concentrations among maternal lines but did observe variation among maternal lines in foliar latex exudation.

Overall, our data reveal powerful genotype‐by‐environment interactions on the expression of most resistance traits in milkweed.

  more » « less
NSF-PAR ID:
10449182
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
11
Issue:
13
ISSN:
2045-7758
Format(s):
Medium: X Size: p. 8542-8561
Size(s):
["p. 8542-8561"]
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ( , Functional Ecology)
    Abstract

    Ecological research has increasingly highlighted the importance of intraspecific variation in shaping the structure and function of communities and ecosystems. Indeed, the effects of intraspecific variation can match or exceed those of interspecific variation. Previous reviews of intraspecific variation in plant traits across heterogeneous environments have focused primarily onmeanphenotypic effects. We propose that a richer and fuller understanding of the ecological causes and consequences of intraspecific variation would be provided by partitioning traitvarianceinto its subcomponents (genetic, environment, genotype by environment interaction).

    We used a meta‐analysis of 352 sets of genetic, environment and genotype by environment (G×E) variation estimates from 72 studies of Salicaceae to compare these sources of variation across plant traits (growth, foliar nitrogen, defence compounds), insect herbivore performance metrics (e.g., survival, growth, fecundity) and environmental conditions (e.g., soil nutrients, water, defoliation).

    Our findings revealed that variation in levels of defence compounds (both condensed tannins and salicinoids) and insect herbivore performance were primarily genetically determined, while variation in plant growth and foliar nitrogen was more environmentally determined.

    Plasticity in plant growth, foliar nitrogen levels and insect herbivore performance varied substantially across different sites (year × location), and nutrient, water and carbon dioxide environments. Plasticity was lowest for chemical defence traits and all traits in contrasting ozone and defoliation environments.

    Our quantitative review also revealed several gaps in the literature, including a need for surveying more mature plants, a wider variety of insect herbivore species (e.g., leaf‐galling insects, specialist insects) and underrepresented environmental treatments (e.g., competition, defoliation, disease, light and water availability).

    Findings from this analysis highlight the importance of, and patterns within, intraspecific variation with respect to shaping the evolvability and plasticity of traits and governing the interactions of plants and insects.

    Aplain language summaryis available for this article.

     
    more » « less
  2. ; ; ; ( , Evolution)
    Abstract

    A major predicted constraint on the evolution of anti-herbivore defense in plants is the nonindependent expression of traits mediating resistance. Since herbivore attack can be highly variable across plant tissues, we hypothesized that correlations in toxin expression within and between plant tissues may limit population differentiation and, thus, plant adaptation. Using full-sib families from two nearby (<1 km) common milkweed (Asclepias syriaca) populations, we investigated genetic correlations among 28 distinct cardenolide toxins within and between roots, leaves, and seeds and examined signatures of tissue-specific divergent selection between populations by QST–FST comparisons. The prevalence, direction, and strength of genetic correlations among cardenolides were tissue specific, and concentrations of individual cardenolides were moderately correlated between tissues; nonetheless, the direction and strength of correlations were population specific. Population divergence in the cardenolide chemistry was stronger in roots than in leaves and seeds. Divergent selection on individual cardenolides was tissue and toxin specific, except for a single highly toxic cardenolide (labriformin), that showed divergent selection across all plant tissues. Heterogeneous evolution of cardenolides within and between tissues across populations appears possible due to their highly independent expression. This independence may be common in nature, especially in specialized interactions in which distinct herbivores feed on different plant tissues.

     
    more » « less
  3. ; ; ( , New Phytologist)
    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. ; ; ; ; ; ; ; ; ; ; et al ( , Ecology)
    Abstract

    Efforts to maintain the function of critical ecosystems under climate change often begin with foundation species. In the southwestern United States, cottonwood trees support diverse communities in riparian ecosystems that are threatened by rising temperatures. Genetic variation within cottonwoods shapes communities and ecosystems, but these effects may be modified by phenotypic plasticity, where genotype traits change in response to environmental conditions. Here, we investigated plasticity in Fremont cottonwood (Populus fremontii) leaf litter traits as well as the consequences of plasticity for riparian ecosystems. We used three common gardens each planted with genotypes from six genetically divergent populations spanning a 12°C temperature gradient, and a decomposition experiment in a common stream environment. We found that leaf litter area, specific leaf area, and carbon to nitrogen ratio (C:N) were determined by interactions between genetics and growing environment, as was the subsequent rate of litter decomposition. Most of the genetic variation in leaf litter traits appeared among rather than within source populations with distinct climate histories. Source populations from hotter climates generally produced litter that decomposed more quickly, but plasticity varied the magnitude of this effect. We also found that hotter growing conditions reduced the variation in litter traits produced across genotypes, homogenizing the litter inputs to riparian ecosystems. All genotypes in the hottest garden produced comparatively small leaves that decomposed quickly and supported lower abundances of aquatic invertebrates, whereas the same genotypes in the coldest garden produced litter with distinct morphologies and decomposition rates. Our results suggest that plastic responses to climate stress may constrict the expression of genetic variation in predictable ways that impact communities and ecosystems. Understanding these interactions between genetic and environmental variation is critical to our ability to plan for the role of foundation species when managing and restoring riparian ecosystems in a warming world.

     
    more » « less
  5. ; ; ; ; ; ; ; ( , Journal of Animal Ecology)
    Abstract

    Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterfliesDanaus plexippus, consistently experience infection by a virulent parasiteOphryocystis elektroscirrha, and some medicinal milkweed (Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity.

    We investigated plant‐mediated influences of elevated CO2(eCO2) on endogenous immune responses of monarch larvae to infection byO. elektroscirrha. Recently, transcriptomics have revealed that infection byO. elektroscirrhadoes not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO2lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO2alter the balance between exogenous and endogenous sources of immunity remains unknown.

    We fed monarchs two species of milkweed;A. curassavica(medicinal) andA. incarnata(non‐medicinal) grown under ambient CO2(aCO2) or eCO2. We then measured endogenous immune responses (phenoloxidase activity, haemocyte concentration and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions.

    The melanization response of late‐instar larvae was reduced on medicinal milkweed in comparison to non‐medicinal milkweed. Moreover, the endogenous immune responses of early‐instar larvae to infection byO. elektroscirrhawere generally lower in larvae reared on foliage from aCO2plants and higher in larvae reared on foliage from eCO2plants. When grown under eCO2, milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO2results in increased endogenous immune function.

    Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.

     
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email