skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Can disease resistance evolve independently at different ages? Genetic variation in age‐dependent resistance to disease in three wild plant species
Abstract Juveniles are typically less resistant (more susceptible) to infectious disease than adults, and this difference in susceptibility can help fuel the spread of pathogens in age‐structured populations. However, evolutionary explanations for this variation in resistance across age remain to be tested.One hypothesis is that natural selection has optimized resistance to peak at ages where disease exposure is greatest. A central assumption of this hypothesis is that hosts have the capacity to evolve resistance independently at different ages. This would mean that host populations have (a) standing genetic variation in resistance at both juvenile and adult stages, and (b) that this variation is not strongly correlated between age classes so that selection acting at one age does not produce a correlated response at the other age.Here we evaluated the capacity of three wild plant species (Silene latifolia,S. vulgarisandDianthus pavonius) to evolve resistance to their anther‐smut pathogens (Microbotryumfungi), independently at different ages. The pathogen is pollinator transmitted, and thus exposure risk is considered to be highest at the adult flowering stage.Within each species we grew families to different ages, inoculated individuals with anther smut, and evaluated the effects of age, family and their interaction on infection.In two of the plant species,S. latifoliaandD. pavonius, resistance to smut at the juvenile stage was not correlated with resistance to smut at the adult stage. In all three species, we show there are significant age × family interaction effects, indicating that age specificity of resistance varies among the plant families.Synthesis. These results indicate that different mechanisms likely underlie resistance at juvenile and adult stages and support the hypothesis that resistance can evolve independently in response to differing selection pressures as hosts age. Taken together our results provide new insight into the structure of genetic variation in age‐dependent resistance in three well‐studied wild host–pathogen systems.  more » « less
Award ID(s):
1936334
PAR ID:
10371126
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Ecology
Volume:
110
Issue:
9
ISSN:
0022-0477
Page Range / eLocation ID:
p. 2046-2061
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary The mechanisms underlying trait conservation over long evolutionary time scales are poorly known. These mechanisms fall into the two broad and nonmutually exclusive categories of constraint and selection. A variety of factors have been hypothesized to constrain trait evolution. Alternatively, selection can maintain similar trait values across many species if the causes of selection are also relatively conserved, while many sources of constraint may be overcome over longer periods of evolutionary divergence. An example of deep trait conservation is tetradynamy in the large family Brassicaceae, where the four medial stamens are longer than the two lateral stamens. Previous work has found selection to maintain this difference in lengths, which we call anther separation, in wild radish,Raphanus raphanistrum.Here, we test the constraint hypothesis using five generations of artificial selection to reduce anther separation in wild radish.We found a rapid linear response to this selection, with no evidence for depletion of genetic variation and correlated responses to this selection in only four of 15 other traits, suggesting a lack of strong constraint.Taken together, available evidence suggests that tetradynamy is likely to be conserved due to selection, but the function of this trait remains unclear. 
    more » « less
  2. Abstract Spatial partitioning is a classic hypothesis to explain plant species coexistence, but evidence linking local environmental variation to spatial sorting, demography and species' traits is sparse. If co‐occurring species' performance is optimized differently along environmental gradients because of trait variation, then spatial variation might facilitate coexistence.We used a system of four naturally co‐occurring species ofClarkia(Onagraceae) to ask whether distribution patchiness corresponds to variation in two environmental variables that contribute to hydrological variation. We then reciprocally sowedClarkiainto each patch type and measured demographic rates in the absence of congeneric competition. Species sorted in patches along one or both gradients, and in three of the four species, germination rate in the ‘home’ patch was higher than all other patches.Spatially variable germination resulted in the same three species exhibiting the highest population growth rates in their home patches.Species' trait values related to plant water use, as well as indicators of water stress in home patches, differed among species and corresponded to home patch attributes. However, post‐germination survival did not vary among species or between patch types, and fecundity did not vary spatially.Synthesis. Our research demonstrates the likelihood that within‐community spatial heterogeneity affects plant species coexistence, and presents novel evidence that differential performance in space is explained by what happens in the germination stage. Despite the seemingly obvious link between adult plant water‐use and variation in the environment, our results distinguish the germination stage as important for spatially variable population performance. 
    more » « less
  3. Innate, infection-preventing resistance often varies between host life stages. Juveniles are more resistant than adults in some species, whereas the opposite pattern is true in others. This variation cannot always be explained by prior exposure or physiological constraints and so it has been hypothesized that trade-offs with other life-history traits may be involved. However, little is known about how trade-offs between various life-history traits and resistance at different life stages affect the evolution of age-specific resistance. Here, we use a mathematical model to explore how trade-offs with natural mortality, reproduction and maturation combine to affect the evolution of resistance at different life stages. Our results show that certain combinations of trade-offs have substantial effects on whether adults or juveniles are more resistant, with trade-offs between juvenile resistance and adult reproduction inherently more costly than trade-offs involving maturation or mortality (all else being equal), resulting in consistent evolution of lower resistance at the juvenile stage even when infection causes a lifelong fecundity reduction. Our model demonstrates how the differences between patterns of age-structured resistance seen in nature may be explained by variation in the trade-offs involved and our results suggest conditions under which trade-offs tend to select for lower resistance in juveniles than adults. 
    more » « less
  4. Summary Phenotypic plasticity allows organisms to optimize traits for their environment. As organisms age, they experience diverse environments that benefit from varying degrees of phenotypic plasticity. Developmental transitions can control these age‐dependent changes in plasticity, and as such, the timing of these transitions can determine when plasticity changes in an organism.Here, we investigate how the transition from juvenile‐to adult‐vegetative development known as vegetative phase change (VPC) contributes to age‐dependent changes in phenotypic plasticity and how the timing of this transition responds to environment using both natural accessions and mutant lines in the model plantArabidopsis thaliana.We found that the adult phase of vegetative development has greater plasticity in leaf morphology than the juvenile phase and confirmed that this difference in plasticity is caused by VPC using mutant lines. Furthermore, we found that the timing of VPC, and therefore the time when increased plasticity is acquired, varies significantly across genotypes and environments.The consistent age‐dependent changes in plasticity caused by VPC suggest that VPC may be adaptive. This genetic and environmental variation in the timing of VPC indicates the potential for population‐level adaptive evolution of VPC. 
    more » « less
  5. 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