skip to main content


Title: The nutritional landscape of host plants for a specialist insect herbivore
Abstract

Nutrition has far‐reaching effects on both the ecology and evolution of species. A substantial body of work has examined the role of host plant quality on insect herbivores, with a particular focus on specialist–generalist dynamics, the interaction of growth and other physiological attributes on fitness and tritrophic effects. Measures of plant quality usually involve one or two axes of nutritional space: typically secondary metabolites or elemental proxies (N and C) of protein and carbohydrates, respectively.

Here, we describe the nutrient space of seven host plants of the specialist insect herbivore,Manduca sexta, using an approach that measures physiologically relevant sources of nutrition, soluble protein and digestible carbohydrates. We show that plant species differ markedly in their nutrient content, offering developing insect herbivores a range of available nutrient spaces that also depend on the age of the leaves being consumed.

The majority of host‐plant species produce diets that are suboptimal to the herbivore, likely resulting in varying levels of compensatory feeding forM. sextato reach target levels of protein to ensure successful growth and development. Low‐quality diets can also impact immune function leading to complex patterns of optimization of plant resources that maximizes both growth and the ability to defend from parasitoids and pathogens. This study is the first to quantify the nutrient space of a suite of host plants used by an insect herbivore using physiologically relevant measures of nutrition.

 
more » « less
NSF-PAR ID:
10460576
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
9
Issue:
23
ISSN:
2045-7758
Page Range / eLocation ID:
p. 13104-13113
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships.

    To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory byManduca sexta, and the attraction of a parasitoid wasp,Cotesia congregata.

    Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks.

    Plant cultivars had different levels of resistance to herbivory byM. sexta, but this did not depend on plant domestication or soil type. The parasitoidC. congregatawas primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil.

    Synthesis.These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions.

     
    more » « less
  2. Abstract

    Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L‐tyrosine and its role as a defence against herbivores.

    We examined overexpression of tyrosine in 97 species ofInga(Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti‐herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations.

    Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L‐tyrosine,Ingaspecies with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine‐producing species also contained secondary metabolites that are derived from tyrosine: tyrosine‐gallates, tyramine‐gallates and DOPA‐gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants.

    Synthesis. We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti‐herbivore defences.

     
    more » « less
  3. Abstract

    Access to high‐quality food is a main driver of population dynamics. For herbivores, protein and carbohydrates are key nutrients that are notoriously variable in plants and are affected by land use. However, few studies have linked foraging decisions and performance in the laboratory to the nutritional landscape available in the field.

    Oedaleus senegalensisis a non‐model locust, a grass‐feeder, and the main pest of millet, a subsistence crop in the Sahel. In this study, we examined dietary preference and locust performance across a range of protein:carbohydrate ratios using the Geometric Framework methodology. We then applied a fitness landscape approach to visualize these results with the plant nutrient contents available across four land‐use types: millet, groundnut, fallow, and grazed fields. Finally, we contrasted our results with locust distribution in the field. Several locust species (O. senegalensisincluded) exhibit density‐dependent colour polymorphism; thus, we also reported individual coloration (brown or green).

    We found thatO. senegalensispreferred moderately carbohydrate‐biased food 1:1.6 protein:carbohydrate ratio. All traits recorded (mass gain, development time, growth rate, moult success and performance index) were best near that ratio and declined on either side presenting a ‘hump‐shape’. Fallow fields contained more plants, particularly grasses, that were both abundant and closer to the optimal protein:carbohydrate ratio recorded from the laboratory experiments.

    When we surveyedO. senegalensisabundance and proportion, we found that they were more numerous in the fallow fields. Brown morph individuals, the ones associated with high density, were proportionally more abundant in fallow fields than green individuals.

    Our study provides evidence that variation in nutritional landscapes – relative to an herbivore's optimal nutrient balance – is a key driver of herbivore population distribution and abundance, and can be used to predict bottom‐up effects on herbivore species.

     
    more » « less
  4. 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
  5. Abstract

    Nitrogen limitation theory predicts that terrestrial plants should benefit from nitrogen inputs and that herbivores should benefit from subsequent higher plant protein contents. While this pattern has generally been supported, some herbivorous insects have shown preference and higher performance on low protein (p), high carbohydrate (c) diets as juveniles.

    However, little is known about the effects on reproduction in adults. Using nitrogen fertilizer, we demonstrate that high plant p:c has negative effects on Senegalese locust (Orthoptera:Oedaeleus senegalensis) reproduction and survival in an agroecological setting.

    For this, we measured p:c in millet plantsPennisetum glaucumthat received two levels of fertilizer (high and moderate) and a control, then we caged locusts on these plants for 2 weeks. In the laboratory, we gave locusts the choice between untreated millet leaves and leaves that received one of the two fertilization treatment.

    We found that fertilization increased p:c ratio in a concentration‐dependent fashion. We counted the number of locusts alive over the course of 2 weeks and showed that fewer females survived on fertilized plants than on control plants. Females that ate plants from the high fertilization treatment laid lighter eggs. Finally, we showed that female locusts prefer unfertilized plants to plants with a high p:c.

    We hypothesize that this pattern will apply broadly to species that have extensive carbohydrate needs, such as long‐distance migrators. Because many ecological studies focus primarily on nitrogen or protein, and fail to consider carbohydrates, this study has important implications for how ecologists consider nutrient limitation of primary consumers in ecosystems globally.

     
    more » « less