skip to main content


Title: Gillespie eco‐evolutionary models ( GEM s) reveal the role of heritable trait variation in eco‐evolutionary dynamics
Abstract

Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco‐evolutionary models usually fail to track how variation changes through time. Moreover, eco‐evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco‐evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco‐evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function.GEMs work by adding a trait distribution component to the standard Gillespie algorithm – an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrateGEMs with the Rosenzweig–MacArthur consumer–resource model. We show not only how heritable trait variation fuels trait evolution and influences eco‐evolutionary dynamics, but also how the erosion of variation through time may hinder eco‐evolutionary dynamics in the long run.GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expectGEMs will open the door to a new direction in eco‐evolutionary and evolutionary modeling by removing long‐standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco‐evolutionary treatment of a greater diversity of ecological interactions. These factors makeGEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.

 
more » « less
NSF-PAR ID:
10196913
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
6
Issue:
4
ISSN:
2045-7758
Page Range / eLocation ID:
p. 935-945
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Evolution is a fundamentally population level process in which variation, drift and selection produce both temporal and spatial patterns of change. Statistical model fitting is now commonly used to estimate which kind of evolutionary process best explains patterns of change through time using models like Brownian motion, stabilizing selection (Ornstein–Uhlenbeck) and directional selection on traits measured from stratigraphic sequences or on phylogenetic trees. But these models assume that the traits possessed by a species are homogeneous. Spatial processes such as dispersal, gene flow and geographical range changes can produce patterns of trait evolution that do not fit the expectations of standard models, even when evolution at the local‐population level is governed by drift or a typicalOUmodel of selection. The basic properties of population level processes (variation, drift, selection and population size) are reviewed and the relationship between their spatial and temporal dynamics is discussed. Typical evolutionary models used in palaeontology incorporate the temporal component of these dynamics, but not the spatial. Range expansions and contractions introduce rate variability into drift processes, range expansion under a drift model can drive directional change in trait evolution, and spatial selection gradients can create spatial variation in traits that can produce long‐term directional trends and punctuation events depending on the balance between selection strength, gene flow, extirpation probability and model of speciation. Using computational modelling that spatial processes can create evolutionary outcomes that depart from basic population‐level notions from these standard macroevolutionary models.

     
    more » « less
  2. Summary

    Predicting the fate of coastal marshes requires understanding how plants respond to rapid environmental change. Environmental change can elicit shifts in trait variation attributable to phenotypic plasticity and act as selective agents to shift trait means, resulting in rapid evolution. Comparably, less is known about the potential for responses to reflect the evolution of trait plasticity.

    Here, we assessed the relative magnitude of eco‐evolutionary responses to interacting global change factors using a multifactorial experiment. We exposed replicates of 32Schoenoplectus americanusgenotypes ‘resurrected’ from century‐long, soil‐stored seed banks to ambient or elevated CO2, varying levels of inundation, and the presence of a competing marsh grass, across two sites with different salinities.

    Comparisons of responses to global change factors among age cohorts and across provenances indicated that plasticity has evolved in five of the seven traits measured. Accounting for evolutionary factors (i.e. evolution and sources of heritable variation) in statistical models explained an additional 9–31% of trait variation.

    Our findings indicate that evolutionary factors mediate ecological responses to environmental change. The magnitude of evolutionary change in plant traits over the last century suggests that evolution could play a role in pacing future ecosystem response to environmental change.

     
    more » « less
  3. Abstract

    The leaf economic spectrum is a widely studied axis of plant trait variability that defines a trade‐off between leaf longevity and productivity. While this has been investigated at the global scale, where it is robust, and at local scales, where deviations from it are common, it has received less attention at the intermediate scale of plant functional types (PFTs). We investigated whether global leaf economic relationships are also present within the scale of plant functional types (PFTs) commonly used by Earth System models, and the extent to which this global‐PFThierarchy can be used to constrain trait estimates. We developed a hierarchical multivariate Bayesian model that assumes separate means and covariance structures within and acrossPFTs and fit this model to seven leaf traits from theTRYdatabase related to leaf longevity, morphology, biochemistry, and photosynthetic metabolism. Although patterns of trait covariation were generally consistent with the leaf economic spectrum, we found three approximate tiers to this consistency. Relationships among morphological and biochemical traits (specific leaf area [SLA], N, P) were the most robust within and acrossPFTs, suggesting that covariation in these traits is driven by universal leaf construction trade‐offs and stoichiometry. Relationships among metabolic traits (dark respiration [Rd], maximum RuBisCo carboxylation rate [Vc,max], maximum electron transport rate [Jmax]) were slightly less consistent, reflecting in part their much sparser sampling (especially for high‐latitudePFTs), but also pointing to more flexible plasticity in plant metabolistm. Finally, relationships involving leaf lifespan were the least consistent, indicating that leaf economic relationships related to leaf lifespan are dominated by across‐PFTdifferences and that within‐PFTvariation in leaf lifespan is more complex and idiosyncratic. Across all traits, this covariance was an important source of information, as evidenced by the improved imputation accuracy and reduced predictive uncertainty in multivariate models compared to univariate models. Ultimately, our study reaffirms the value of studying not just individual traits but the multivariate trait space and the utility of hierarchical modeling for studying the scale dependence of trait relationships.

     
    more » « less
  4. Abstract

    Flowering time and water‐use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time,WUE, andWUEplasticity to drought inArabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) IsWUEplasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions ofA. thalianagrown in well‐watered and season‐ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment.WUEand flowering time were consistently positively genetically correlated.WUEwas correlated withWUEplasticity, but the direction changed between treatments. Selection generally favored early flowering and lowWUE, with drought favoring earlier flowering significantly more than well‐watered conditions. Selection for lowerWUEwas marginally stronger under drought. There were no net fitness costs ofWUEplasticity.WUEplasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation betweenWUEand flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions ofA. thaliana.WUEplasticity may be favored over completely fixed development in environments with periodic drought.

     
    more » « less
  5. Abstract

    Floral attraction traits can significantly affect pollinator visitation patterns, but adaptive evolution of these traits may be constrained by correlations with other traits. In some cases, molecular pathways contributing to floral attraction are well characterized, offering the opportunity to explore loci potentially underlying variation among individuals. Here, we quantify the range of variation in floralUVpatterning (i.e.UV‘bulls‐eye nectar guides) among crop and wild accessions ofBrassica rapa. We then use experimental crosses to examine the genetic architecture, candidate loci and biochemical underpinnings of this patterning as well as phenotypic manipulations to test the ecological impact. We find qualitative variation inUVpatterning between wild (commonly lackingUVpatterns) and crop (commonly exhibitingUVpatterns) accessions. Similar to the majority of crops, recombinant inbred lines (RILs) derived from an oilseed crop × WIfast‐plant®cross exhibitUVpatterns, the size of which varies extensively among genotypes. InRILs, we further observe strong statistical‐genetic andQTLcorrelations within petal morphological traits and within measurements of petalUVpatterning; however, correlations between morphology andUVpatterning are weak or nonsignificant, suggesting thatUVpatterning is regulated and may evolve independently of overall petal size.HPLCanalyses reveal a high concentration of sinapoyl glucose inUV‐absorbing petal regions, which, in concert with physical locations ofUV‐traitQTLs, suggest a regulatory and structural gene as candidates underlying observed quantitative variation. Finally, insects prefer flowers withUVbulls‐eye patterns over those that lack patterns, validating the importance ofUVpatterning in pollen‐limited populations ofB. rapa.

     
    more » « less