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Dormancy has repeatedly evolved in plants, animals, and microbes and is hypothesized to facilitate persistence in the face of environmental change. Yet previous experiments have not tracked demography and trait evolution spanning a full successional cycle to ask whether early bouts of natural selection are later reinforced or erased during periods of population dormancy. In addition, it is unclear how well short-term measures of fitness predict long-term genotypic success for species with dormancy. Here, we address these issues using experimental field populations of the plantOenothera biennis, which evolved over five generations in plots exposed to or protected from insect herbivory. While populations existed above ground, there was rapid evolution of defensive and life-history traits, but populations lost genetic diversity and crashed as succession proceeded. After >5 y of seed dormancy, we triggered germination from the seedbank and genotyped >3,000 colonizers. Resurrected populations showed restored genetic diversity that reduced earlier responses to selection and pushed population phenotypes toward the starting conditions of a decade earlier. Nonetheless, four defense and life-history traits remained differentiated in populations with insect suppression compared with controls. These findings capture key missing elements of evolution during ecological cycles and demonstrate the impact of dormancy on future evolutionary responses to environmental change.
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Evolutionary effects of nitrogen are not easily predicted from ecological responses
Anthropogenic nitrogen (N) addition might alter the evolutionary trajectories of plant populations, in part because it alters the abiotic and biotic environment by increasing aboveground primary productivity, light asymmetry, and herbivory intensity, and reducing plant species diversity. Such evolutionary impacts could be caused by N altering patterns of natural selection (i.e., trait-fitness relationships) and the opportunity for selection (i.e., variance in relative fitness). Because at the community level N addition favors species with light acquisition strategies (e.g., tall species), we predict that N would also increase selection favoring those same traits. We also hypothesize that N could alter the opportunity for selection via its effects on mean fitness and/or competitive asymmetries.To investigate these evolutionary consequences of N, we quantified the strength of selection and the opportunity for selection in replicated populations of the annual grass Setaria faberi Herrm. (giant foxtail) growing in a long-term N addition experiment. We also correlated our measures of selection and opportunity for selection with light asymmetry, diversity, and herbivory intensity to identify the proximate causes of any N effects on evolutionary processes. N addition increased aboveground productivity, light asymmetry, and reduced species diversity. Contrary to expectations, N addition did not strengthen selection for trait values associated with higher light acquisition such as greater height and specific leaf area (SLA); rather, it strengthened selection favoring lower SLA. Increased light asymmetry was associated with stronger selection for lower SLA and lower species diversity was associated with stronger selection for greater height and lower SLA, suggesting a role for these factors in driving N-mediated selection. The opportunity for selection was not influenced by N addition (despite increased mean fitness) but was negatively associated with species diversity. Our results indicate that anthropogenic N enrichment can affect evolutionary processes, but that evolutionary changes in plant traits within populations are unlikely to parallel the shifts in plant traits observed at the community level. Data was collected in 2020 from a field experiment in a long-term ecological research site (Kellogg Biological Station LTER site in Michigan, USA). The Data folder contains 3 separate datasets as CSV files, each with accompanying .txt metadata files: 1) a dataset of individual-level data (Waterton2022_NitrogenEvolution_Individual_Data.csv); 2) a dataset of annual net primary productivity (ANPP; Waterton2022_NitrogenEvolution_ANPP_Data.csv); 3) a dataset of light measurements (Waterton2022_NitrogenEvolution_Light_Data.csv). An R script for reproducing the analyses and figures is available at https://doi.org/10.5281/zenodo.7121361. R statistical software is required to run the R script.
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- Award ID(s):
- 1832042
- PAR ID:
- 10464869
- Publisher / Repository:
- Dryad
- Date Published:
- Edition / Version:
- 6
- Subject(s) / Keyword(s):
- Nitrogen enrichment phenotypic selection opportunity for selection light asymmetry species diversity herbivory Setaria faberi LTER Poaceae FOS: Biological sciences
- Format(s):
- Medium: X Size: 99820 bytes
- Size(s):
- 99820 bytes
- Sponsoring Org:
- National Science Foundation
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Abstract Ecological theory predicts that herbivory should be weaker on islands than on mainland based on the assumption that islands have lower herbivore abundance and diversity. However, empirical tests of this prediction are rare, especially for insect herbivores, and those few tests often fail to address the mechanisms behind island–mainland divergence in herbivory. In particular, past studies have not addressed the relative contribution of top‐down (i.e. predator‐driven) and bottom‐up (i.e. plant‐driven) factors to these dynamics.To address this, we experimentally excluded insectivorous vertebrate predators (e.g. birds, bats) and measured leaf traits associated with herbivory in 52 populations of 12 oak (Quercus) species in three island–mainland sites: The Channel Islands of California vs. mainland California, Balearic Islands vs. mainland Spain, and the island Bornholm vs. mainland Sweden (N = 204 trees). In each site, at the end of the growing season, we measured leaf damage by insect herbivores on control vs. predator‐excluded branches and measured leaf traits, namely: phenolic compounds, specific leaf area, and nitrogen and phosphorous content. In addition, we obtained climatic and soil data for island and mainland populations using global databases. Specifically, we tested for island–mainland differences in herbivory, and whether differences in vertebrate predator effects or leaf traits between islands and mainland contributed to explaining the observed herbivory patterns.Supporting predictions, herbivory was lower on islands than on mainland, but only in the case of Mediterranean sites (California and Spain). We found no evidence for vertebrate predator effects on herbivory on either islands or mainland in any study site. In addition, while insularity affected leaf traits in some of the study sites (Sweden‐Bornholm and California), these effects were seemingly unrelated to differences in herbivory.Synthesis. Our results suggest that vertebrate predation and the studied leaf traits did not contribute to island–mainland variation patterns in herbivory, calling for more nuanced and comprehensive investigations of predator and plant trait effects, including measurements of other plant traits and assessments of predation by different groups of natural enemies.more » « less
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Abstract Selection causes local adaptation across populations within species and simultaneously divergence between species. However, it is unclear if either the force of or the response to selection is similar across these scales. We show that natural selection drives divergence between closely related species in a pattern that is distinct from local adaptation within species. We use reciprocal transplant experiments across three species ofPhloxwildflowers to characterize widespread adaptive divergence. Using provenance trials, we also find strong local adaptation between populations within a species. Comparing divergence and selection between these two scales of diversity we discover that one suite of traits predicts fitness differences between species and that an independent suite of traits predicts fitness variation within species. Selection drives divergence between species, contributing to speciation, while simultaneously favoring extensive diversity that is maintained across populations within a species. Our work demonstrates how the selection landscape is complex and multidimensional.more » « less
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{"Abstract":["Evolutionary adaptation can allow a population to persist in the face of a\n new environmental challenge. With many populations now threatened by\n environmental change, it is important to understand whether this process\n of evolutionary rescue is feasible under natural conditions, yet work on\n this topic has been largely theoretical. We used unique long-term data to\n parameterize deterministic and stochastic models of the contribution of\n one trait to evolutionary rescue using field estimates for the subalpine\n plant Ipomopsis aggregata and hybrids with its close relative I.\n tenuituba. In the absence of evolution or plasticity, the two studied\n populations are projected to go locally extinct due to earlier snowmelt\n under climate change, which imposes drought conditions. Phenotypic\n selection on specific leaf area (SLA) was estimated in 12 years and\n multiple populations. Those data on selection and its environmental\n sensitivity to annual snowmelt timing in the spring were combined with\n previous data on heritability of the trait, phenotypic plasticity of the\n trait, and the impact of snowmelt timing on mean absolute fitness.\n Selection favored low values of SLA (thicker leaves). The evolutionary\n response to selection on that single trait was insufficient to allow\n evolutionary rescue by itself, but in combination with phenotypic\n plasticity it promoted evolutionary rescue in one of the two populations.\n The number of years until population size would stop declining and begin\n to rise again was heavily dependent upon stochastic environmental changes\n in snowmelt timing around the trend line. Our study illustrates how field\n estimates of quantitative genetic parameters can be used to predict the\n likelihood of evolutionary rescue. Although a complete set of parameter\n estimates are generally unavailable, it may also be possible to predict\n the general likelihood of evolutionary rescue based on published ranges\n for phenotypic selection and heritability and the extent to which early\n snowmelt impacts fitness."],"Methods":["The study sites consisted of three “Poverty Gulch” sites in\n Gunnsion National Forest and one site “Vera Falls” at the Rocky Mountain\n Biological Laboratory, all in Gunnison County, CO, USA. Focal plants\n included two sets of plants. One set (data from 2009-2019) consisted of\n plants in common gardens at three sites: an I. aggregata\n site (hereafter “agg”), an I. tenuituba\n site (hereafter “ten”) and a site at the center of the natural\n hybrid zone (hereafter “hyb”). The second set consisted of plants growing\n in situ at two of the same Poverty Gulch sites (“agg” and “hyb”), and\n an I. aggregata site at Vera Falls (hereafter “VF”;\n data from 2017-2023). The common gardens were started\n from seed in 2007 and 2008. Measurements of SLA in these gardens began\n when plants were 2 years old, either 2009 or 2010 depending upon the\n garden, as they are only small seedlings during their first summer after\n seed maturation. By 2018, all but 15 of the 4512 plants originally planted\n had died, with or without blooming, and we stopped following these\n gardens. Starting in 2017, in situ vegetative plants at the I.\n aggregata site and the hybrid site whose longest leaf exceeded\n 25 mm were marked with metal tags to facilitate\n identification. In each year of the study, one leaf\n from each vegetative plant was collected in the field and transported on\n ice to the RMBL, 8 km distant. There each leaf was scanned with a flatbed\n scanner and analyzed using ImageJ to measure leaf area. The leaf was dried\n at 70 deg C for 2 hours and then weighed to obtain dry mass and calculate\n SLA as area/dry mass. For plants in the common gardens, SLA was measured\n on 982 leaves from 383 plants in 2009 – 2014. For in situ plants, SLA was\n measured on one leaf from each of 877 plants in 2017 – 2022. Fitness was\n estimated as the binary variable of survival to flowering. Plants that\n were still alive in 2019 in the common gardens or in 2023 at the end of\n the study were assumed to survive to flowering. These\n data were used to estimate selection differentials on SLA in each of 12\n years. We then combined this information with previous information on\n heritability and the effect of snowmelt date in the spring on mean\n absolute fitness, measured as the finite rate of population increase, from\n a previous demographic study. This information was used to parameterize\n models of evolutionary rescue that we developed. We developed two models\n that differed in how snowmelt timing changed: a Step-change model and a\n Gradual environmental change model and analyzed both deterministic and\n stochastic versions. All analysis and modeling was done in R ver\n 4.2.2. "],"TechnicalInfo":["# Data for: Predicting the contribution of single trait evolution to\n rescuing a plant population from demographic impacts of climate change\n Dataset DOI: [10.5061/dryad.ht76hdrtn](10.5061/dryad.ht76hdrtn) ##\n Description of the data and file structure File\n "mastervegtraitsSLA2023.csv" contains data on specific leaf area\n for Ipomopsis plants in the field. Files\n "masterdemography_insitu_2023.csv" and\n "masterdemography_commongarden.csv" provide the corresponding\n information on survival to flowering. File "snowmelt.csv"\n provides dates of snowmelt in the spring. File\n "selection_vs_snowmelt.csv" provides intermediate results on\n selection intensities from analysis with the first parts of the code\n "Campbell-EvolutionLettersMay2025.Rmd". File\n "IPMresults.csv" provides estimates of the finite rate of\n increase (lambda) predicted from the publication by Campbell\n [https://doi.org/10.1073/pnas.1820096116](https://doi.org/10.1073/pnas.1820096116) File "Campbell-EvolutionLettersMay2025.Rmd" provides the R code for statistical analysis and the deterministic and stochastic models of evolutionary rescue. All data analysis and modeling was done in R ver. 4.4.2 on a Windows machine. All necessary input data files are provided. The R code is annotated to indicate which portions produce analyses and figures in the manuscript. For the multipart figures 6-9 the code needs to be manually updated to produce each part of the figure before assembling them. In those cases, each part represents a model with a unique set of parameters. ### Files and variables #### File: Data\\_files\\_for\\_EVL\\_Campbell\\_2025.zip **Description:** All data files Blank cells are indicated by "." except in "selection_vs_snowmelt.csv" where they are indicated by "NA" **File:** mastervegtraitsSLA2023.csv * meltday = first day of bare ground at the Rocky Mountain Biological Lab (RMBL) in units of days starting with January 1 * year = year * site = site. agg = site with I. aggregata. hyb = site with natural hybrids. ten = site with I. tenuituba. VF = Vera Falls site containing I. aggregata. * idtag = metal tag used to identify plant * planttype = type of plant. AA = progeny of I. aggregata x I. aggregata. AT = progeny of I. aggregata x I. tenuituba. TA = progeny of I. tenuituba x I. aggregata. TT = progeny of I. tenuituba x I. tenuituba. F2 = progeny of F1 (either AT or TA) x F1. agg = natural I. aggregata. hyb = natural hybrid. * sla = specific leaf area in units of cm2/g * uniqueid = an id used to identify the plant uniquely across all years and sites **File:** masterdemography\\_insitu\\_2023.csv * site = site. agg = site with I. aggregata. hyb = site with hybrids. VF = Vera Falls site containing I. aggregata. * idtag = metal tag used to identify plant * yeartagged = year the plant was first tagged * flrlabelxx = label for plants flowering in year 20xx * stagexxxx = stage in year xxxx. 0 = dead. 1 = single vegetative rosette. 2 = single inflorescence. 3 = multiple vegetative rosette. 4 = multiple inflorescence. * lengthxx = length of longest leaf in year 20xx in mm * leavesxx = number of leaves in rosette(s) in year 20xx **File:** masterdemography_commongarden.csv * site = site. agg = site with I. aggregata. hyb = site with natural hybrids. ten = site with I. tenuituba. * IDTAG = metal tag used to identify plant * Planttype = type of plant. AA = progeny of I. aggregata x I. aggregata. AT = progeny of I. aggregata x I. tenuituba. TA = progeny of I. tenuituba x I. aggregata. TT = progeny of I. tenuituba x I. tenuituba. F2full = full-sib progeny of F1 (either AT or TA) x F1. F2non = non full-sib progeny of F1 x F1. * stagexx = stage of plant in year 20xx. 0 = dead. 1 = single vegetative rosette. 2 = single inflorescence. 3 = multiple vegetative rosette. 4 = multiple inflorescence. * lengthxx = length of longest leaf in year 20xx in mm. * leavesxx = number of leaves in rosette(s) in year 20xx. **File:** snowmelt.csv * Year = year * Snowmelt = day of first bare ground at the RMBL in units of day starting with January 1. Values prior to 1975 were estimated. **File:** selection*vs*snowmelt.csv * meltday = day of first bare ground at the RMBL in units of day starting with January 1. * year = year * Sbyyearwithsite = standardized selection differential on SLA in model that includes site. These values are reproduced with standard errors in Table 1. * bwithsite = regression coefficient for raw survival on raw SLA in model that includes site. * meansurv = mean survival * covwsla = raw selection differential on SLA * bwithsitehyb = regression coefficient for raw survival on SLA at site hyb * meansurvhyb = mean survival at site hyb * covwslahyb = raw selection differential on SLA at site hyb used in the Gradual environmental change model * covwslaagg = raw selection differential on SLA at site agg used in the Gradual environmental change model * meansurvagg = mean survival at site agg * melthyb = estimated date of bare ground at site hyb * meltagg = estimated date of bare ground at site agg **File:** IPMresults.csv * site = site. agg = site with I. aggregata. hyb = site with natural hybrids. * day = predicted day of snowmelt (all predictions are from Campbell, D. R. 2019. Early snowmelt projected to cause population decline in a subalpine plant. PNAS (USA) 116(26) 1290-12906.) Units are days starting with January 1. * lambda = predicted finite rate of increase **File:** Campbell-EvolutionLettersMay2025.Rmd Contains R code for data analysis and modeling. All analysis and modeling was done in R ver 4.2.2."]}more » « less
