skip to main content

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


  • NSF Public Access
  • Search Results
  • Phenological and fitness responses to climate warming depend upon genotype and competitive neighbourhood in Arabidopsis thaliana
Title: Phenological and fitness responses to climate warming depend upon genotype and competitive neighbourhood in Arabidopsis thaliana
Abstract

Increasing temperatures during climate change are known to alter the phenology across diverse plant taxa, but the evolutionary outcomes of these shifts are poorly understood. Moreover, plant temperature‐sensing pathways are known to interact with competition‐sensing pathways, yet there remains little experimental evidence for how genotypes varying in temperature responsiveness react to warming in realistic competitive settings.

We compared flowering time and fitness responses to warming and competition for two near‐isogenic lines (NILs) ofArabidopsis thalianatransgressively segregating temperature‐sensitive and temperature‐insensitive alleles for major‐effect flowering time genes. We grew focal plants of each genotype in intraspecific and interspecific competition in four treatments contrasting daily temperature profiles in summer and fall under contemporary and warmed conditions. We measured phenology and fitness of focal plants to quantify plastic responses to season, temperature and competition and the dependence of these responses on flowering time genotype.

The temperature‐insensitive NIL was constitutively early flowering and less fit, except in a future‐summer climate in which its fitness was higher than the later flowering, temperature‐sensitive NIL in low competition. The late‐flowering NIL showed accelerated flowering in response to intragenotypic competition and to increased temperature in the summer but delayed flowering in the fall. However, its fitness fell with rising temperatures in both seasons, and in the fall its marginal fitness gain from decreasing competition was diminished in the future.

Functional alleles at temperature‐responsive genes were necessary for plastic responses to season, warming and competition. However, the plastic genotype was not the most fit in every experimental condition, becoming less fit than the temperature‐canalized genotype in the warm summer treatment.

Climate change is often predicted to have deleterious effects on plant populations, and our results show how increased temperatures can act through genotype‐dependent phenology to decrease fitness. Furthermore, plasticity is not necessarily adaptive in rapidly changing environments since a nonplastic genotype proved fitter than a plastic genotype in a warming climate treatment.

Aplain language summaryis available for this article.

  more » « less
Award ID(s):
1754102
PAR ID:
10462882
Author(s) / Creator(s):
 ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Functional Ecology
Volume:
33
Issue:
2
ISSN:
0269-8463
Page Range / eLocation ID:
p. 308-322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ( , Functional Ecology)
    Abstract

    In Mediterranean climates, the timing of seasonal rains determines germination, flowering phenology and fitness. As climate change alters seasonal precipitation patterns, it is important to ask how these changes will affect the phenology and fitness of plant populations. We addressed this question experimentally with the annual plant speciesArabidopsis thaliana.

    In a first experiment, we manipulated the date of rainfall onset and recorded germination phenology on sand and soil substrates. In a second experiment, we manipulated germination date, growing season length and mid‐season drought to measure their effects on flowering time and fitness. Within each experiment, we manipulated seed dormancy and flowering time using multilocus near‐isogenic lines segregating strong and weak alleles of the seed dormancy geneDOG1and the flowering time geneFRI. We synthesized germination phenology data from the first experiment with fitness functions from the second experiment to project population fitness under different seasonal rainfall scenarios.

    Germination phenology tracked rainfall onset but was slower and more variable on sand than on soil. Many seeds dispersed on sand in spring and summer delayed germination until the cooler temperatures of autumn. The high‐dormancyDOG1allele also prevented immediate germination in spring and summer. Germination timing strongly affected plant fitness. Fecundity was highest in the October germination cohort and declined in spring germinants. The late floweringFRIallele had lower fecundity, especially in early fall and spring cohorts. Projections of population fitness revealed that: (1) Later onset of autumn rains will negatively affect population fitness. (2) Slow, variable germination on sand buffers populations against fitness impacts of variable spring and summer rainfall. (3) Seasonal selection favours high dormancy and early flowering genotypes in a Mediterranean climate with hot dry summers. The high‐dormancyDOG1allele delayed germination of spring‐dispersed fresh seeds until more favourable early fall conditions, resulting in higher projected population fitness.

    These findings suggest that Mediterranean annual plant populations are vulnerable to changes in seasonal precipitation, especially in California where rainfall onset is already occurring later. The fitness advantage of highly dormant, early flowering genotypes helps explain the prevalence of this strategy in Mediterranean populations.

    Read the freePlain Language Summaryfor this article on the Journal blog.

     
    more » « less
  2. ; ; ; ; ; ; ; ; ; ; et al ( , New Phytologist)
    Summary

    Plant phenology, the timing of recurrent biological events, shows key and complex response to climate warming, with consequences for ecosystem functions and services. A key challenge for predicting plant phenology under future climates is to determine whether the phenological changes will persist with more intensive and long‐term warming.

    Here, we conducted a meta‐analysis of 103 experimental warming studies around the globe to investigate the responses of four phenophases – leaf‐out, first flowering, last flowering, and leaf coloring.

    We showed that warming advanced leaf‐out and flowering but delayed leaf coloring across herbaceous and woody plants. As the magnitude of warming increased, the response of most plant phenophases gradually leveled off for herbaceous plants, while phenology responded in proportion to warming in woody plants. We also found that the experimental effects of warming on plant phenology diminished over time across all phenophases. Specifically, the rate of changes in first flowering for herbaceous species, as well as leaf‐out and leaf coloring for woody species, decreased as the experimental duration extended.

    Together, these results suggest that the real‐world impact of global warming on plant phenology will diminish over time as temperatures continue to increase.

     
    more » « less
  3. ; ; ( , PLANTS, PEOPLE, PLANET)
    Societal Impact Statement

    Networks of digitized herbarium records are rich resources for understanding plant responses to climate change. While the climate is warming globally, some localities are experiencing climate cooling, the effects of which are poorly understood. Our herbarium‐based study of a geographically restricted species shows that the timing of reproduction can shift earlier as the climate becomes cooler and wetter. Local variation in climate change may be a key factor driving the high variability of changes observed in plant reproduction and climate cooling should be considered along with other global change drivers. This will help enable accurate predictions for the successful management of climate change effects.

    Summary

    Plant phenological responses to global warming are well studied. However, while many locations are experiencing increased temperatures, some locations are experiencing climate cooling. Little work has been conducted to understand plant phenological responses to cooling trends, much less the combined effects of cooling and other factors, such as changing precipitation. Furthermore, studies based on herbarium specimens have been instrumental in demonstrating plant responses to global warming; but to our knowledge, herbarium records have not been used to investigate responses to cooling.

    We collected data from 98 years of herbarium records to evaluate whether the reproductive phenology (flowering/fruiting) of an annual mustard, cedar gladecress (Leavenworthia stylosa), has changed as the climate has become cooler and wetter in central Tennessee, USA. Additionally, we conducted two field experiments to assess reproductive consequences of different flowering times.

    Over the last century, gladecress reproductive phenology has shifted 2.1 days earlier per decade, concurrent with wetter conditions during germination and cooler conditions during reproduction. Field experiments showed that plants with extremely early and moderately early flowering had equivalent reproduction, but these plants had greater reproduction than intermediate‐ and late‐flowering plants.

    Counter to expectations from global warming studies, our work demonstrates that climate cooling and greater rainfall can result in earlier plant reproductive phenology, potentially due to asymmetric selection for early flowering. Future studies may need to consider climate cooling along with other global change factors to fully explain changes in plant phenology. Our understanding of plant responses to climate cooling can be enhanced through additional herbarium‐based research.

     
    more » « less
  4. ; ; ; ; ; ; ; ; ( , New Phytologist)
    Summary

    The relevance of flowering time variation and plasticity to climate adaptation requires a comprehensive empirical assessment. We investigated natural selection and the genetic architecture of flowering time in Arabidopsis through field experiments in Europe across multiple sites and seasons.

    We estimated selection for flowering time, plasticity and canalization. Loci associated with flowering time, plasticity and canalization by genome‐wide association studies were tested for a geographic signature of climate adaptation.

    Selection favored early flowering and increased canalization, except at the northernmost site, but was rarely detected for plasticity. Genome‐wide association studies revealed significant associations with flowering traits and supported a substantial polygenic inheritance. Alleles associated with late flowering, including functionalFRIGIDAvariants, were more common in regions experiencing high annual temperature variation. Flowering time plasticity to fall vs spring and summer environments was associated withGIGANTEA SUPPRESSOR 5, which promotes early flowering under decreasing day length and temperature.

    The finding that late flowering genotypes and alleles are associated with climate is evidence for past adaptation. Real‐time phenotypic selection analysis, however, reveals pervasive contemporary selection for rapid flowering in agricultural settings across most of the species range. The response to this selection may involve genetic shifts in environmental cuing compared to the ancestral state.

     
    more » « less
  5. ; ; ; ( , Scientific Reports)
    Abstract

    Interspecific competition reduces resource availability and can affect evolution. We quantified multivariate selection in the presence and absence of strong interspecific competition using a greenhouse experiment with 35 natural accessions ofArabidopsis thaliana. We assessed selection on nine traits representing plant phenology, growth, and architecture, as well as their plasticities.Competition reduced biomass and fitness by over 98%, and plastic responses to competition varied by genotype (significant G × E) for all traits except specific leaf area (SLA). Competitive treatments altered selection on flowering phenology and plant architecture, with significant selection on all phenology traits and most architecture traits under competition-present conditions but little indication that selection occurred in the absence of competitors. Plasticity affected fitness only in competition-present conditions, where plasticity in flowering time and early internode lengths was adaptive. The competitive environment caused changes in the trait correlation structure and surprisingly reduced phenotypic integration, which helped explain some of the observed selection patterns. Despite this overall shift in the trait correlation matrix, genotypes with delayed flowering had lower SLA (thicker, tougher leaves) regardless of the competitive environment, a pattern we have not seen previously reported in the literature. Overall, our study highlights multiple ways in which interspecific competition can alter selective regimes, contributing to our understanding of variability in selection processes over space and time.

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