Variation and plasticity in life-history traits and fitness of wild Arabidopsis thaliana populations are not related to their genotypic and ecological diversity.
Arabidopsis thaliana
Common garden experiment
Phenotypic plasticity
Phenotypic variation
Within-population variation
Journal
BMC ecology and evolution
ISSN: 2730-7182
Titre abrégé: BMC Ecol Evol
Pays: England
ID NLM: 101775613
Informations de publication
Date de publication:
03 May 2024
03 May 2024
Historique:
received:
19
01
2024
accepted:
25
04
2024
medline:
4
5
2024
pubmed:
4
5
2024
entrez:
3
5
2024
Statut:
epublish
Résumé
Despite its implications for population dynamics and evolution, the relationship between genetic and phenotypic variation in wild populations remains unclear. Here, we estimated variation and plasticity in life-history traits and fitness of the annual plant Arabidopsis thaliana in two common garden experiments that differed in environmental conditions. We used up to 306 maternal inbred lines from six Iberian populations characterized by low and high genotypic (based on whole-genome sequences) and ecological (vegetation type) diversity. Low and high genotypic and ecological diversity was found in edge and core Iberian environments, respectively. Given that selection is expected to be stronger in edge environments and that ecological diversity may enhance both phenotypic variation and plasticity, we expected genotypic diversity to be positively associated with phenotypic variation and plasticity. However, maternal lines, irrespective of the genotypic and ecological diversity of their population of origin, exhibited a substantial amount of phenotypic variation and plasticity for all traits. Furthermore, all populations harbored maternal lines with canalization (robustness) or sensitivity in response to harsher environmental conditions in one of the two experiments. Overall, we conclude that the environmental attributes of each population probably determine their genotypic diversity, but all populations maintain substantial phenotypic variation and plasticity for all traits, which represents an asset to endure in changing environments.
Sections du résumé
BACKGROUND
BACKGROUND
Despite its implications for population dynamics and evolution, the relationship between genetic and phenotypic variation in wild populations remains unclear. Here, we estimated variation and plasticity in life-history traits and fitness of the annual plant Arabidopsis thaliana in two common garden experiments that differed in environmental conditions. We used up to 306 maternal inbred lines from six Iberian populations characterized by low and high genotypic (based on whole-genome sequences) and ecological (vegetation type) diversity.
RESULTS
RESULTS
Low and high genotypic and ecological diversity was found in edge and core Iberian environments, respectively. Given that selection is expected to be stronger in edge environments and that ecological diversity may enhance both phenotypic variation and plasticity, we expected genotypic diversity to be positively associated with phenotypic variation and plasticity. However, maternal lines, irrespective of the genotypic and ecological diversity of their population of origin, exhibited a substantial amount of phenotypic variation and plasticity for all traits. Furthermore, all populations harbored maternal lines with canalization (robustness) or sensitivity in response to harsher environmental conditions in one of the two experiments.
CONCLUSIONS
CONCLUSIONS
Overall, we conclude that the environmental attributes of each population probably determine their genotypic diversity, but all populations maintain substantial phenotypic variation and plasticity for all traits, which represents an asset to endure in changing environments.
Identifiants
pubmed: 38702598
doi: 10.1186/s12862-024-02246-x
pii: 10.1186/s12862-024-02246-x
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
56Subventions
Organisme : Agencia Estatal de Investigación of Spain
ID : PID2022-136893NB-I00
Organisme : Agencia Estatal de Investigación of Spain
ID : CGL2016-77720-P
Informations de copyright
© 2024. The Author(s).
Références
Carley LN, Morris WF, Walsh R, Riebe D, Mitchell-Olds T. Are genetic variation and demographic performance linked? Evol Appl. 2022;15:1888–906. https://doi.org/10.1111/eva.13487 .
doi: 10.1111/eva.13487
pubmed: 36426131
pmcid: 9679243
Chevin LM, Lande R, Mace GM. Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biol. 2010;8:e1000357. https://doi.org/10.1371/journal.pbio.1000357 .
doi: 10.1371/journal.pbio.1000357
pubmed: 20463950
pmcid: 2864732
Frankham R. Relationship of genetic variation to population size in wildlife. Conserv Biol. 1996;10:1500–8. https://doi.org/10.1046/j.1523-1739.1996.10061500.x .
doi: 10.1046/j.1523-1739.1996.10061500.x
Leimu R, Mutikainen P, Koricheva J, Fischer M. How general are positive relationships between plant population size, fitness and genetic variation? J Ecol. 2006;94:942–52. https://doi.org/10.1111/j.1365-2745.2006.01150.x .
doi: 10.1111/j.1365-2745.2006.01150.x
Butlin RK, Tregenza T. Levels of genetic polymorphism: marker loci versus quantitative traits. Phil Trans R Soc Lond B. 1998;353:187–98. https://doi.org/10.1098/2Frstb.1998.0201 .
doi: 10.1098/2Frstb.1998.0201
Reed DH, Frankham R. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis Evolution. 2001;55:1095–103. https://doi.org/10.1111/j.0014-3820.2001.tb00629.x .
doi: 10.1111/j.0014-3820.2001.tb00629.x
pubmed: 11475045
McKay JK, Latta RG. Adaptive population divergence: markers QTL and traits. Trends Ecol Evol. 2002;17:285–91. https://doi.org/10.1016/S0169-5347(02)02478-3 .
doi: 10.1016/S0169-5347(02)02478-3
Villellas J, Berjano R, Terrab A, Garcia MB. Divergence between phenotypic and genetic variation within populations of a common herb across Europe. Ecosphere. 2014;5:56. https://doi.org/10.1890/ES13-00291.1 .
doi: 10.1890/ES13-00291.1
Volis S, Ormanbekova D, Yermekbayev K, Song M, Shulgina I. The conservation value of peripheral populations and a relationship between quantitative trait and molecular variation. Evol Biol. 2016;43:26–36. https://doi.org/10.1007/s11692-015-9346-3 .
doi: 10.1007/s11692-015-9346-3
Walisch TJ, Colling G, Hermant S, Matthies D. Molecular and quantitative genetic variation within and between populations of the declining grassland species Saxifraga granulata. Ecol Evol. 2022;12:e9462. https://doi.org/10.1002/ece3.9462 .
doi: 10.1002/ece3.9462
pubmed: 36415877
pmcid: 9674452
Castilla AR, Méndez-Vigo B, Marcer A, Martínez-Minaya J, Conesa D, Picó FX, et al. Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana. BMC Evol Biol. 2020;20:71. https://doi.org/10.1186/s12862-020-01635-2 .
doi: 10.1186/s12862-020-01635-2
pubmed: 32571210
pmcid: 7310121
Lundemo S, Falahati-Anbaran M, Stenøien HK. Seed banks cause elevated generation times and effective population sizes of Arabidopsis thaliana in northern Europe. Mol Ecol. 2009;18:2798–811. https://doi.org/10.1111/j.1365-294x.2009.04236.x .
doi: 10.1111/j.1365-294x.2009.04236.x
pubmed: 19500249
Bomblies K, Yant L, Laitinen RA, Kim ST, Hollister JD, Warthmann N, et al. Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet. 2010;6:e1000890. https://doi.org/10.1371/journal.pgen.1000890 .
doi: 10.1371/journal.pgen.1000890
pubmed: 20361058
pmcid: 2845663
Falahati-Anbaran M, Lundemo S, Stenøien HK. Seed dispersal in time can counteract the effect of gene flow between natural populations of Arabidopsis thaliana. New Phytol. 2014;202:1043–54. https://doi.org/10.1111/nph.12702 .
doi: 10.1111/nph.12702
pubmed: 24471774
Méndez-Vigo B, Castilla AR, Gómez R, Marcer A, Alonso-Blanco C, Picó FX. Spatiotemporal dynamics of genetic variation at the quantitative and molecular levels within a natural Arabidopsis thaliana population. J Ecol. 2022;110:2701–16. https://doi.org/10.1111/1365-2745.13981 .
doi: 10.1111/1365-2745.13981
Galloway LF. Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytol. 2005;166:93–100. https://doi.org/10.1111/j.1469-8137.2004.01314.x .
doi: 10.1111/j.1469-8137.2004.01314.x
pubmed: 15760354
Chevin LM, Lande R. Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J Evol Biol. 2011;24:1462–76. https://doi.org/10.1111/j.1420-9101.2011.02279.x .
doi: 10.1111/j.1420-9101.2011.02279.x
pubmed: 21545421
Matesanz S, Ramírez-Valiente JA. A review and meta-analysis of intraspecific differences in phenotypic plasticity: Implications to forecast plant responses to climate change. Global Ecol Biogeogr. 2019;28:1682–94. https://doi.org/10.1111/geb.12972 .
doi: 10.1111/geb.12972
Pironon S, Papuga G, Villellas J, Angert AL, García MB, Thompson JD. Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biol Rev Camb Philos Soc. 2017;92:1877–909. https://doi.org/10.1111/brv.12313 .
doi: 10.1111/brv.12313
pubmed: 27891813
Bontrager M, Usui T, Lee-Yaw JA, Anstett DN, Branch HA, Hargreaves AL, et al. Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion. Evolution. 2021;75:1316–33. https://doi.org/10.1111/evo.14231 .
doi: 10.1111/evo.14231
pubmed: 33885152
Gomaa NH, Montesinos-Navarro A, Alonso-Blanco C, Picó FX. Temporal variation in genetic diversity and effective population size of Mediterranean and subalpine Arabidopsis thaliana populations. Mol Ecol. 2011;20:3540–54. https://doi.org/10.1111/j.1365-294x.2011.05193.x .
doi: 10.1111/j.1365-294x.2011.05193.x
pubmed: 21790818
Montesinos-Navarro A, Wig J, Picó FX, Tonsor ST. Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol. 2011;189:282–94. https://doi.org/10.1111/j.1469-8137.2010.03479.x .
doi: 10.1111/j.1469-8137.2010.03479.x
pubmed: 20880224
Vidigal DS, Marques ACSS, Willems LAJ, Buijs G, Méndez-Vigo M, Hilhorst HWM, et al. Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana. Plant Cell Environ. 2016;39:1737–48. https://doi.org/10.1111/pce.12734 .
doi: 10.1111/pce.12734
pubmed: 26991665
Picó FX. Demographic fate of Arabidopsis thaliana cohorts of autumn- and spring-germinated plants along an altitudinal gradient. J Ecol. 2012;100:1009–18. https://doi.org/10.1111/j.1365-2745.2012.01979.x .
doi: 10.1111/j.1365-2745.2012.01979.x
Argyres AZ, Schmitt J. Microgeographic genetic structure of morphological and life history traits in a natural population of Impatiens capensis. Evolution. 1991;45:175–89. https://doi.org/10.1111/j.1558-5646.1991.tb05276.x .
doi: 10.1111/j.1558-5646.1991.tb05276.x
Galloway LF. Response to natural environmental heterogeneity: Maternal effects and selection on life-history characters and plasticities in Mimulus guttatus. Evolution. 1995;49:1095–107. https://doi.org/10.2307/2410434 .
doi: 10.2307/2410434
pubmed: 28568540
Prati D, Schmid B. Genetic differentiation of life-history traits within populations of the clonal plant Ranunculus reptans. Oikos. 2000;90:442–56. https://doi.org/10.1034/j.1600-0706.2000.900303.x .
doi: 10.1034/j.1600-0706.2000.900303.x
Weinig C, Dorn LA, Kane NC, German ZM, Halldorsdottir SS, Ungerer MC, et al. Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics. 2003;165:321–9. https://doi.org/10.1093/genetics/165.1.321 .
doi: 10.1093/genetics/165.1.321
pubmed: 14504239
pmcid: 1462755
Paccard A, Vance M, Willi Y. Weak impact of fine-scale landscape heterogeneity on evolutionary potential in Arabidopsis lyrata. J Evol Biol. 2013;26:2331–40. https://doi.org/10.1111/jeb.12220 .
doi: 10.1111/jeb.12220
pubmed: 23980569
Callahan HS, Pigliucci M. Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. Ecology. 2002;83:1965–80. https://doi.org/10.2307/3071779 .
doi: 10.2307/3071779
Lázaro-Nogal A, Matesanz S, Godoy A, Pérez-Trautman F, Gianoli E, Valladares F. Environmental heterogeneity leads to higher plasticity in dry-edge populations of a semi-arid Chilean shrub: insights into climate change responses. J Ecol. 2015;103:338–50. https://doi.org/10.1111/1365-2745.12372 .
doi: 10.1111/1365-2745.12372
de la Mata R, Zas R, Bustingorri G, Sampedro L, Rust M, Hernandez-Serrano A, et al. Drivers of population differentiation in phenotypic plasticity in a temperate conifer: A 27-year study. Evol Appl. 2022;15:1945–62. https://doi.org/10.1111/eva.13492 .
doi: 10.1111/eva.13492
pubmed: 36426125
pmcid: 9679231
Galloway LF, Etterson JR. Transgenerational plasticity is adaptive in the wild. Science. 2007;318:1134–6. https://doi.org/10.1126/science.1148766 .
doi: 10.1126/science.1148766
pubmed: 18006745
Auge GA, Leverett LD, Edwards BR, Donohue K. Adjusting phenotypes via within- and across-generational plasticity. New Phytol. 2017;216:343–9. https://doi.org/10.1111/nph.14495 .
doi: 10.1111/nph.14495
pubmed: 28262950
Schmid MW, Heichinger C, Coman Schmid D, Guthörl D, Gagliardini V, Bruggmann R, et al. Contribution of epigenetic variation to adaptation in Arabidopsis. Nat Commun. 2018;9:4446. https://doi.org/10.1038/s41467-018-06932-5 .
doi: 10.1038/s41467-018-06932-5
pubmed: 30361538
pmcid: 6202389
Yan Z, Tian D, Han W, Ji C, Hou X, Guo Y, et al. Weak transgenerational effects of ancestral nitrogen and phosphorus availabilities on offspring phenotypes in Arabidopsis thaliana. J Plant Res. 2023;136:515–25. https://doi.org/10.1007/s10265-023-01456-6 .
doi: 10.1007/s10265-023-01456-6
pubmed: 37055608
Picó FX, Méndez-Vigo B, Martínez-Zapater JM, Alonso-Blanco C. Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian Peninsula. Genetics. 2008;180:1009–21. https://doi.org/10.1534/genetics.108.089581 .
doi: 10.1534/genetics.108.089581
pubmed: 18716334
pmcid: 2567352
Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C. Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC and PHYC genes in Arabidopsis. Plant Physiol. 2011;157:1942–55. https://doi.org/10.1104/pp.111.183426 .
doi: 10.1104/pp.111.183426
pubmed: 21988878
pmcid: 3327218
Manzano-Piedras E, Marcer A, Alonso-Blanco C, Picó FX. Deciphering the adjustment between environment and life history in annuals: lessons from a geographically-explicit approach in Arabidopsis thaliana. PLoS ONE. 2014;9:e87836. https://doi.org/10.1371/journal.pone.0087836 .
doi: 10.1371/journal.pone.0087836
pubmed: 24498381
pmcid: 3912251
Marcer A, Vidigal DS, James PMA, Fortin MJ, Méndez-Vigo B, Hilhorst HWM, et al. Temperature fine-tunes Mediterranean Arabidopsis thaliana life-cycle phenology geographically. Plant Biol. 2018;20:148–56. https://doi.org/10.1111/plb.12558 .
doi: 10.1111/plb.12558
pubmed: 28241389
Tabas-Madrid D, Méndez-Vigo B, Arteaga N, Marcer A, Pascual-Montano A, Weigel D, et al. Genome-wide signatures of flowering adaptation to climate temperature: Regional analyses in a highly diverse native range of Arabidopsis thaliana. Plant Cell Environ. 2018;41:1806–20. https://doi.org/10.1111/pce.13189 .
doi: 10.1111/pce.13189
pubmed: 29520809
Rueden C, Schindelin TJ, Hiner MC, DeZonia BE, Walter AE, Arena ET, et al. Image J2: ImageJ for the next generation of scientific image data. BMC Bioinformatics. 2017;18:529. https://doi.org/10.1186/s12859-017-1934-z .
doi: 10.1186/s12859-017-1934-z
pubmed: 29187165
pmcid: 5708080
Exposito-Alonso M, Brennan AC, Alonso-Blanco C, Picó FX. Spatio-temporal variation in fitness responses to contrasting environments in Arabidopsis thaliana. Evolution. 2018;72:1570–86. https://doi.org/10.1111/evo.13508 .
doi: 10.1111/evo.13508
Gómez R, Méndez-Vigo B, Marcer A, Alonso-Blanco C, Picó FX. Quantifying temporal change in plant population attributes: insights from a resurrection approach. AoB Plants. 2018;10:ply063. https://doi.org/10.1093/aobpla/ply063 .
doi: 10.1093/aobpla/ply063
pubmed: 30370042
pmcid: 6198925
Stoler N, Nekrutenko A. Sequencing error profiles of Illumina sequencing instruments. NAR Genom Bioinform. 2021;27:lqad019. https://doi.org/10.1093/nargab/lqab019 .
doi: 10.1093/nargab/lqab019
SAS. Statistical analysis software. Users’ guide statistics version 9.4. Cary: SAS Institute Inc.; 2013.
Rangel TF, Diniz-Filho JAF, Bini LM. SAM: a comprehensive application for spatial analysis in macroecology. Ecography. 2010;33:46–50. https://doi.org/10.1111/j.1600-0587.2009.06299.x .
doi: 10.1111/j.1600-0587.2009.06299.x
Le Corre V. Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits. Mol Ecol. 2005;14:4181–92. https://doi.org/10.1111/j.1365-294x.2005.02722.x .
doi: 10.1111/j.1365-294x.2005.02722.x
pubmed: 16262868
Valladares F, Sánchez-Gómez D, Zabala MA. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol. 2006;94:1103–16. https://doi.org/10.1111/j.1365-2745.2006.01176.x .
doi: 10.1111/j.1365-2745.2006.01176.x
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48. https://doi.org/10.18637/jss.v067.i01 .
doi: 10.18637/jss.v067.i01
Rosenberg MS, Anderson CD. PASSaGE: Pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods Ecol Evol. 2011;2:229–32. https://doi.org/10.1111/j.2041-210X.2010.00081.x .
doi: 10.1111/j.2041-210X.2010.00081.x
Pebesma E. Simple features for R Standardized support for spatial vector data. The R J. 2018;10:439–46. https://journal.r-project.org/archive/2018/RJ-2018-009/index.html .
doi: 10.32614/RJ-2018-009
Morrissey MB, Sakrejda K. Unification of regression-based methods for the analysis of natural selection. Evolution. 2013;67:2094–100. https://doi.org/10.1111/evo.12077 .
doi: 10.1111/evo.12077
pubmed: 23815662
Vogt G, Huber M, Thiemann M, van den Boogaart G, Schmitz OJ, Schubart CD. Production of different phenotypes from the same genotype in the same environment by developmental variation. J Exp Biol. 2008;211:510–23. https://doi.org/10.1242/jeb.008755 .
doi: 10.1242/jeb.008755
pubmed: 18245627
Debieu M, Tang C, Stich B, Sikosek T, Effgen S, Josephs E, et al. Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. PLoS ONE. 2013;8:e61075. https://doi.org/10.1371/journal.pone.0061075 .
doi: 10.1371/journal.pone.0061075
pubmed: 23717385
pmcid: 3662791
Vasseur F, Exposito-Alonso M, Ayala-Garay OJ, Wang G, Enquist BJ, Vile D, et al. Adaptive diversification of growth allometry in the plant Arabidopsis thaliana. Proc Natl Acad Sci USA. 2018;115:3416–21. https://doi.org/10.1073/pnas.1709141115 .
doi: 10.1073/pnas.1709141115
pubmed: 29540570
pmcid: 5879651
Exposito-Alonso M, 500 Genomes Field Experiment Team, Burbano HA, Bossdorf O, Nielsen R, Weigel D. Natural selection on the Arabidopsis thaliana genome in present and future climates. Nature. 2019;573:126–9. https://doi.org/10.1038/s41586-019-1520-9 .
doi: 10.1038/s41586-019-1520-9
pubmed: 31462776
Martínez-Berdeja A, Stitzer MC, Taylor MA, Okada M, Ezcurra E, Runcie DE, et al. Functional variants of DOG1 control seed chilling responses and variation in seasonal life-history strategies in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2020;117:2526–34. https://doi.org/10.1073/pnas.1912451117 .
doi: 10.1073/pnas.1912451117
pubmed: 31964817
pmcid: 7007534
Stenøien HK, Fenster CB, Tonteri A, Savolainen O. Genetic variability in natural populations of Arabidopsis thaliana in northern Europe. Mol Ecol. 2005;14:137–48. https://doi.org/10.1111/j.1365-294x.2004.02359.x .
doi: 10.1111/j.1365-294x.2004.02359.x
pubmed: 15643957
Frachon L, Libourel C, Villoutreix R, Carrère S, Glorieux C, Huard-Chauveau C, et al. Intermediate degrees of synergistic pleiotropy drive adaptive evolution in ecological time. Nat Eco Evol. 2017;1:1551–61. https://doi.org/10.1038/s41559-017-0297-1 .
doi: 10.1038/s41559-017-0297-1
Murren CJ, Alt CHS, Kohler C, Sancho G. Natural variation on whole-plant form in the wild is influenced by multivariate soil nutrient characteristics: natural selection acts on root traits. Am J Bot. 2020;107:319–28. https://doi.org/10.1002/ajb2.1420 .
doi: 10.1002/ajb2.1420
pubmed: 32002983
Hoffmann AA, Hercus MJ. Environmental stress as an evolutionary force. Bioscience. 2000;50:217–26. https://doi.org/10.1641/0006-3568(2000)050[0217:ESAAEF]2.3.CO;2 .
doi: 10.1641/0006-3568(2000)050[0217:ESAAEF]2.3.CO;2
García-Ramos G, Kirkpatrick M. Genetic models of adaptation and gene flow in peripheral populations. Evolution. 1997;51:21–8. https://doi.org/10.1111/j.1558-5646.1997.tb02384.x- .
doi: 10.1111/j.1558-5646.1997.tb02384.x-
pubmed: 28568782
Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecol Lett. 2004;7:1225–41. https://doi.org/10.1111/j.1461-0248.2004.00684.x .
doi: 10.1111/j.1461-0248.2004.00684.x
Donohue K. Completing the cycle: maternal effects as the missing link in plant life histories. Phil Trans R Soc Lond B. 2009;364:1059–74. https://doi.org/10.1098/rstb.2008.0291 .
doi: 10.1098/rstb.2008.0291
Galloway LF, Burgess KS. Manipulation of flowering time: Phenological integration and maternal effects. Ecology. 2009;90:2139–48. https://doi.org/10.1890/08-0948.1 .
doi: 10.1890/08-0948.1
pubmed: 19739376
Taylor MA, Cooper MD, Sellamuthu R, Braun P, Migneault A, Browning A, et al. Interacting effects of genetic variation for seed dormancy and flowering time on phenology, life history, and fitness of experimental Arabidopsis thaliana populations over multiple generations in the field. New Phytol. 2017;216:291–302. https://doi.org/10.1111/nph.14712 .
doi: 10.1111/nph.14712
pubmed: 28752957
Gomaa NH, Picó FX. Depicting the phenotypic space of the annual plant Diplotaxis acris in hyperarid deserts. Ecol Evol. 2021;11:15708–19. https://doi.org/10.1002/ece3.8232 .
doi: 10.1002/ece3.8232
pubmed: 34824784
pmcid: 8601918
Schmitz G, Linstädter A, Frank ASK, Dittberner H, Thome J, Schrader A, et al. Environmental filtering of life-history trait diversity in urban populations of Arabidopsis thaliana. J Ecol. 2023;112:12–27. https://doi.org/10.1111/1365-2745.14211 .
doi: 10.1111/1365-2745.14211
Fournier-Level A, Wilczek AM, Cooper MD, Roe JL, Anderson J, Eaton D, et al. Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana. Mol Ecol. 2013;22:3552–66. https://doi.org/10.1111/mec.12285 .
doi: 10.1111/mec.12285
pubmed: 23506537
Ågren J, Oakley CG, Lundemo S, Schemske DW. Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping. Evolution. 2017;71:550–64. https://doi.org/10.1111/evo.13126 .
doi: 10.1111/evo.13126
pubmed: 27859214
Postma FM, Ågren J. Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana. Mol Ecol. 2018;27:2498–511. https://doi.org/10.1111/mec.14697 .
doi: 10.1111/mec.14697
pubmed: 29676059
Siepielski AM, DiBattista JD, Carlson SM. It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett. 2009;12:1261–76. https://doi.org/10.1111/j.1461-0248.2009.01381.x .
doi: 10.1111/j.1461-0248.2009.01381.x
pubmed: 19740111
Monro K, Marshall DJ. Faster is not always better: selection on growth rate fluctuates across life history and environments. Am Nat. 2014;183:798–809. https://doi.org/10.1086/676006 .
doi: 10.1086/676006
pubmed: 24823823
Oakley CG, Schemske DW, McKay JK, Ågren J. Ecological genetics of local adaptation in Arabidopsis: An 8-year field experiment. Mol Ecol. 2023;32:4570–83. https://doi.org/10.1111/mec.17045 .
doi: 10.1111/mec.17045
pubmed: 37317048
Ågren J, Oakley CG, McKay JK, Lovell JT, Schemske DW. Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2013;110:21077–82. https://doi.org/10.1073/pnas.1316773110 .
doi: 10.1073/pnas.1316773110
pmcid: 3876199
Lowry DB, Hall MC, Salt DE, Willis JH. Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol. 2009;183:776–88. https://doi.org/10.1111/j.1469-8137.2009.02901.x .
doi: 10.1111/j.1469-8137.2009.02901.x
pubmed: 19549130
Anderson JT, Lee CR, Rushworth CA, Colautti RI, Mitchell-Olds T. Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol Ecol. 2013;22:699–708. https://doi.org/10.1111/j.1365-294x.2012.05522.x .
doi: 10.1111/j.1365-294x.2012.05522.x
pubmed: 22420446
Leinonen PH, Remmington DL, Leppälä J, Savolainen O. Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Mol Ecol. 2013;22:709–23. https://doi.org/10.1111/j.1365-294x.2012.05678.x .
doi: 10.1111/j.1365-294x.2012.05678.x
pubmed: 22724431
Wadgymar SM, Lowry DB, Gould BA, Byron CN, Mactavish RM, Anderson JT. Identifying targets and agents of selection: Innovative methods to evaluate the processes that contribute to local adaptation. Methods Ecol Evol. 2017;8:738–49. https://doi.org/10.1111/2041-210X.12777 .
doi: 10.1111/2041-210X.12777
Wright SJ, Goad DM, Gross BL, Muñoz PR, Olsen KM. Genetic trade-offs underlie divergent life history strategies for local adaptation in white clover. Mol Ecol. 2021;31:3742–60. https://doi.org/10.1111/mec.16180 .
doi: 10.1111/mec.16180
pubmed: 34532899
Rutter MT, Roles AJ, Fenster CB. Quantifying natural seasonal variation in mutation parameters with mutation accumulation lines. Ecol Evol. 2018;8:5575–85. https://doi.org/10.1002/ece3.4085 .
doi: 10.1002/ece3.4085
pubmed: 29938075
pmcid: 6010865
Palacio-Lopez K, Molofsky J. Phenotypic shifts following admixture in recombinant offspring of Arabidopsis thaliana. Evol Ecol. 2021;35:575–93. https://doi.org/10.1007/s10682-021-10118-9 .
doi: 10.1007/s10682-021-10118-9
Méndez-Vigo B, Savic M, Ausín I, Ramiro M, Martín B, Picó FX, et al. Environmental and genetic interactions reveal FLOWERING LOCUS C as a modulator of the natural variation for the plasticity of flowering in Arabidopsis. Plant Cell Environ. 2016;39:282–94. https://doi.org/10.1111/pce.12608 .
doi: 10.1111/pce.12608
pubmed: 26173848
Gianoli E, González-Teuber M. Environmental heterogeneity and population differentiation in plasticity to drought in Convolvulus chilensis (Convolvulaceae). Evol Ecol. 2005;19:603–13. https://doi.org/10.1007/s10682-005-2220-5 .
doi: 10.1007/s10682-005-2220-5
Molina-Montenegro MA, Atala C, Gianoli E. Phenotypic plasticity and performance of Taraxacum officinale (dandelion) in habitats of contrasting environmental heterogeneity. Biol Invasions. 2010;12:2277–84. https://doi.org/10.1007/s10530-009-9638-6 .
doi: 10.1007/s10530-009-9638-6
Gómez-Navarro JJ, Montávez JP, Jiménez-Guerrero P, Jerez S, García-Valero JA, González-Rouco JF. Warming patterns in regional climate change projections over the Iberian Peninsula. Meteorol Z. 2010;19:275–85. https://doi.org/10.1127/0941-2948/2010/0351 .
doi: 10.1127/0941-2948/2010/0351
Alvarez M, Bleich A, Donohue K. Genotypic variation in the persistence of transgenerational responses to seasonal cues. Evolution. 2020;74:2265–80. https://doi.org/10.1111/evo.13996 .
doi: 10.1111/evo.13996
pubmed: 32383475
Montesinos A, Tonsor ST, Alonso-Blanco C, Picó FX. Demographic and genetic patterns of variation among populations of Arabidopsis thaliana from contrasting native environments. PLoS ONE. 2009;4:e7213. https://doi.org/10.1371/journal.pone.0007213 .
doi: 10.1371/journal.pone.0007213
pubmed: 19787050
pmcid: 2746291
Montesinos-Navarro A, Picó FX, Tonsor SJ. Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana. Evolution. 2012;66:3417–31. https://doi.org/10.1111/j.1558-5646.2012.01689.x .
doi: 10.1111/j.1558-5646.2012.01689.x
pubmed: 23106707
Burghardt LT, Jessica C, Metcalf E, Wilczek AM, Schmitt J, Donohue K. Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. Am Nat. 2015;85:212–27. https://doi.org/10.1086/679439 .
doi: 10.1086/679439
Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, et al. Effects of genetic perturbation on seasonal life history plasticity. Science. 2009;323:930–4. https://doi.org/10.1126/science.1165826 .
doi: 10.1126/science.1165826
pubmed: 19150810
Taylor MA, Cooper MD, Schmitt J. Phenological and fitness responses to climate warming depend upon genotype and competitive neighbourhood in Arabidopsis thaliana. Funct Ecol. 2019;33:308–22. https://doi.org/10.1111/1365-2435.13262 .
doi: 10.1111/1365-2435.13262
Scheepens JF, Deng Y, Bossdorf O. Phenotypic plasticity in response to temperature fluctuations is genetically variable, and relates to climatic variability of origin, in Arabidopsis thaliana. AoB Plants. 2018;10:ply043. https://doi.org/10.1093/aobpla/ply043 .
doi: 10.1093/aobpla/ply043
pubmed: 30109013
pmcid: 6084592
Lee U, Mortola EN, Kim EJ, Long M. Evolution and maintenance of phenotypic plasticity. BioSystems. 2022;222:104791. https://doi.org/10.1016/j.biosystems.2022.104791 .
doi: 10.1016/j.biosystems.2022.104791
pubmed: 36244511
Murren CJ. The integrated phenotype. Integr Comp Biol. 2012;52:64–76. https://doi.org/10.1093/icb/ics043 .
doi: 10.1093/icb/ics043
pubmed: 22593559
Huang X, Schmitt J, Dorn L, Griffith C, Effgen S, Takao S, et al. The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy. Mol Ecol. 2010;19:1335–51. https://doi.org/10.1111/j.1365-294x.2010.04557.x .
doi: 10.1111/j.1365-294x.2010.04557.x
pubmed: 20149097
Chiang GCK, Bartsch M, Barua D, Nakabayashi K, Debieu M, Kronholm I, et al. DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Mol Ecol. 2011;20:3336–49. https://doi.org/10.1111/j.1365-294x.2011.05181.x .
doi: 10.1111/j.1365-294x.2011.05181.x
pubmed: 21740475
Groot MP, Kubisch A, Ouborg NJ, Pagel J, Schmid KJ, Vergeer P, et al. Transgenerational effects of mild heat in Arabidopsis thaliana show strong genotype specificity that is explained by climate at origin. New Phytol. 2017;215:1221–34. https://doi.org/10.1111/nph.14642 .
doi: 10.1111/nph.14642
pubmed: 28590553
Zhang YY, Fischer M, Colot V, Bossdorf O. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 2013;197:314–22. https://doi.org/10.1111/nph.12010 .
doi: 10.1111/nph.12010
pubmed: 23121242
Puy J, Carmona CP, Dvořáková H, Latzel V, de Bello F. Diversity of parental environments increases phenotypic variation in Arabidopsis populations more than genetic diversity but similarly affects productivity. Ann Bot. 2021;127:425–36. https://doi.org/10.1093/aob/mcaa100 .
doi: 10.1093/aob/mcaa100
pubmed: 32463878
Picó FX. Variation and plasticity in life-history traits and fitness of wild Arabidopsis thaliana populations are not related to their genotypic and ecological diversity . 2024. Dryad. https://doi.org/10.5061/dryad.98sf7m0qp .