Skip to main content
SpringerLink
Log in

Latitudinal trait variation and responses to drought in Arabidopsis lyrata

  • Population ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Species may respond in three ways to environmental change: adapt, migrate, or go extinct. Studies of latitudinal clines can provide information on whether species have adapted to abiotic stress such as temperature and drought in the past and what the traits underlying adaptation are. We investigated latitudinal trait variation and response to drought in North American populations of Arabidopsis lyrata. Plants from nine populations collected over 13° latitude were grown under well-watered and dry conditions. A total of 1,620 seedlings were raised and 12 phenological, physiological, morphological, and life history traits were measured. Two traits, asymptotic rosette size and the propensity to flower, were significantly associated with latitude: plants from northern locations grew to a larger size and were more likely to flower in the first season. Most traits displayed a plastic response to drought, but plasticity was never related linearly with latitude nor was it enhanced in populations from extreme latitudes with reduced water availability. Populations responded to drought by adopting mixed strategies of resistance, tolerance, and escape. The study shows that latitudinal adaptation in A. lyrata involves the classic life history traits, size at and timing of reproduction. Contrary to recent theoretical predictions, adaptation to margins is based on fixed trait differences and not on phenotypic plasticity, at least with respect to drought.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Al-Shehbaz IA (2010) Magnoliophyta: Salicaceae to Brassicaceae. In: Flora of North America Editorial Committee (eds) Flora of North America north of Mexico. Oxford University Press, New York

  • Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16

    Article  PubMed Central  Google Scholar 

  • Bridle JR, Vines TH (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol Evol 22:140–147

    Article  PubMed  Google Scholar 

  • Chevin LM, Lande R (2011) Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J Evol Biol 24:1462–1476

    Article  PubMed  Google Scholar 

  • Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–251

    Article  CAS  PubMed  Google Scholar 

  • Conover DO, Duffy TA, Hice LA (2009) The covariance between genetic and environmental influences across ecological gradients. Ann NY Acad Sci 1168:100–129

    Article  PubMed  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679

    Article  CAS  PubMed  Google Scholar 

  • De Frenne P, Brunet J, Shevtsova A, Kolb A, Graae BJ, Chabrerie O, Cousins SAO, Decocq G, De Schrijver A, Diekmann M, Gruwez R, Heinken T, Hermy M, Nilsson C, Stanton S, Tack W, Willaert J, Verheyen K (2011) Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient. Glob Change Biol 17:3240–3253

    Article  Google Scholar 

  • Edwards KR, Bastlová D, Edwards-Jonášová M, Kvĕt J (2011) A comparison of univariate and multivariate methods for analyzing clinal variation in an invasive species. Hydrobiologia 674:119–131

    Article  Google Scholar 

  • El-Keblawy A, Lovett-Doust J (1999) Maternal effects in the progeny generation in zucchini, Cucurbita pepo (Cucurbitaceae). Int J Plant Sci 160:331–339

    Article  Google Scholar 

  • Etterson JR (2004) Evolutionary potential of Chamaecrista fasciculata in relation to climate change. I. Clinal patterns of selection along an environmental gradient in the Great Plains. Evolution 58:1446–1458

    Article  PubMed  Google Scholar 

  • Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    Article  CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Franks SJ, Weis AE (2008) A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant. J Evol Biol 21:1321–1334

    Article  CAS  PubMed  Google Scholar 

  • Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711

    Article  CAS  PubMed  Google Scholar 

  • Griffin PC, Willi Y (2014) Evolutionary shifts to self-fertilization restricted to geographic range margins in North American Arabidopsis lyrata. Ecol Lett 17:484–490

    Google Scholar 

  • Griffith TM, Watson MA (2005) Stress avoidance in a common annual: reproductive timing is important for local adaptation and geographic distribution. J Evol Biol 18:1601–1612

    Article  CAS  PubMed  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  CAS  PubMed  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hill WG, Rasbash J (1986a) Models of long term artificial selection in finite population. Genet Res 48:41–50

    Article  CAS  PubMed  Google Scholar 

  • Hill WG, Rasbash J (1986b) Models of long-term artificial selection in finite population with recurrent mutation. Genet Res 48:125–131

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9:421–432

    Article  CAS  PubMed  Google Scholar 

  • Jenkins DG, Carey M, Czerniewska J, Fletcher J, Hether T et al (2010) A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography 33:315–320

    Google Scholar 

  • Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020

    Article  Google Scholar 

  • Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342

    Article  Google Scholar 

  • Kincaid DT, Schneider RB (1983) Quantification of leaf shape with a microcomputer and Fourier transform. Can J Bot 61:2333–2342

    Article  Google Scholar 

  • Knight CA, Vogel H, Kroymann J, Shumate A, Witsenboer H, Mitchell-Olds T (2006) Expression profiling and local adaptation of Boechera holboellii populations for water use efficiency across a naturally occurring water stress gradient. Mol Ecol 15:1229–1237

    Article  CAS  PubMed  Google Scholar 

  • Ludlow MM (1989) Strategies of response to water stress. In: Kreeb KH, Richter H, Hinckley TM (eds) Structural and functional responses to environmental stresses: water shortage. SPB, the Hague, pp 269–281

    Google Scholar 

  • Lynch M, Lande R (1993) Evolution and extinction in response to environmental change. In: Kareiva PM, Kingsolver JG, Huey RB (eds) Biotic interactions and global change. Sinauer, Sunderland, pp 234–250

    Google Scholar 

  • Maherali H, Reid CD, Polley HW, Johnson HB, Jackson RB (2002) Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ 25:557–566

    Article  CAS  Google Scholar 

  • Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  • Maron JL, Elmendorf SC, Vilà M (2007) Contrasting plant physiological adaptation to climate in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924

    Article  PubMed  Google Scholar 

  • McKay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana. 1. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12:1137–1151

    Article  CAS  PubMed  Google Scholar 

  • Neuffer B (2011) Native range variation in Capsella bursa-pastoris (Brassicaceae) along a 2500 km latitudinal transect. Flora 206:107–119

    Article  Google Scholar 

  • Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38:535–552

    Article  Google Scholar 

  • Novy A, Flory SL, Hartman JM (2013) Evidence for rapid evolution of phenology in an invasive grass. J Evol Biol 26:443–450

    Article  CAS  PubMed  Google Scholar 

  • Paccard A, Vance M, Willi Y (2013) Weak impact of fine-scale landscape heterogeneity on evolutionary potential in Arabidopsis lyrata. J Evol Biol 26:2331–2340

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Pickett STA (1989) Space-for-time substitution as an alternative to long-term studies. In: Likens GE (ed) Long-term studies in ecology: approaches and alternatives. Springer, New York Berlin Heidelberg, pp 110–135

    Chapter  Google Scholar 

  • Picotte JJ, Rhode JM, Cruzan MB (2009) Leaf morphological responses to variation in water availability for plants in the Piriqueta caroliniana complex. Plant Ecol 200:267–275

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rasband WS (2011) ImageJ. US National Institutes of Health, Bethesda, MD. http://imagej.nih.gov/ij/

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riihimäki M, Podolsky R, Kuittinen H, Koelewijn H, Savolainen O (2005) Studying genetics of adaptive variation in model organisms: flowering time variation in Arabidopsis lyrata. Genetica 123:63–74

    Article  PubMed  Google Scholar 

  • Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22

    Google Scholar 

  • Robertson A (1960) A theory of limits in artificial selection. Proc R Soc Lond B 153:234–249

    Article  Google Scholar 

  • SAS Institute (2002) SAS: version 9.2. SAS Institute, Cary, NC

  • Schmickl R, Jørgensen MH, Brysting AK, Koch MA (2010) The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evol Biol 10:98

    Article  PubMed Central  PubMed  Google Scholar 

  • Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436

    Article  Google Scholar 

  • Singer JD (1998) Using SAS PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. J Educ Behav Stat 24:323–355

    Article  Google Scholar 

  • Sletvold N, Ågren J (2012) Variation in tolerance to drought among Scandinavian populations of Arabidopsis lyrata. Evol Ecol 26:559–577

    Article  Google Scholar 

  • Steets JA, Takebayashi N, Byrnes JM, Wolf DE (2010) Heterogeneous selection on trichome production in Alaskan Arabidopsis kamchatica (Brassicaceae). Am J Bot 97:1098–1108

    Article  PubMed  Google Scholar 

  • Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101:4712–4717

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trabucco A, Zomer RJ (2010) Global soil water balance geospatial database. CGIAR Consortium for Spatial Information. Available at: http://www.cgiar-csi.org

  • Travis SE, Grace JB (2010) Predicting performance for ecological restoration: a case study using Spartina alterniflora. Ecol Appl 20:192–204

    Article  PubMed  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Wei M, Caballero A, Hill WG (1996) Selection response in finite populations. Genetics 144:1961–1974

    CAS  PubMed Central  PubMed  Google Scholar 

  • Willi Y, Hoffmann AA (2009) Demographic factors and genetic variation influence population persistence under environmental change. J Evol Biol 22:124–133

    Article  PubMed  Google Scholar 

  • Willi Y, Määttänen K (2010) Evolutionary dynamics of mating system shifts in Arabidopsis lyrata. J Evol Biol 23:2123–2131

    Article  CAS  PubMed  Google Scholar 

  • Willi Y, Määttänen K (2011) The relative importance of factors determining genetic drift: mating system, spatial genetic structure, habitat and census size in Arabidopsis lyrata. New Phytol 189:1200–1209

    Article  PubMed  Google Scholar 

  • Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecol Monogr 82:149–168

    Article  Google Scholar 

  • Wu CA, Lowry DB, Nutter LI, Willis JH (2010) Natural variation for drought-response traits in the Mimulus guttatus species complex. Oecologia 162:23–33

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Collection permits were granted by the US Army at Fort Leonard Wood, the Iowa State Preserves Advisory Board, the Iowa Department of Natural Resources, the Virginia Department of Conservation and Recreation, the Nature Conservancy of Maryland, the US National Park Service, and the New York State Office of Parks. Seeds at Fort Leonard Wood were kindly sampled by Joe Proffitt. We would like to thank the many people who helped with measuring plants, Olivier Bachmann, Emmanuel Bonjour, Benjamin Dauphin, Philippa Griffin, Adnan Peco, Marta Anda Perez, Katia Presani, Anouk Sarr, Reyhan Sonmez, and Julien Vieu. Josh Van Buskirk provided comments on the manuscript. Mass spectrometry was performed at the University of New Hampshire Stable Isotope Laboratory, Durham, NH, USA, and the Cornell University Stable Isotope Laboratory, Ithaca, NY, USA. The research was supported by the Swiss National Science Foundation (PP00P3-123396/1) and the Fondation Pierre Mercier pour la Science. The experiments were performed in Switzerland and comply with the current laws of this country.

Author information

Authors and Affiliations

  1. Evolutionary Botany, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, 2000, Neuchâtel, Switzerland

    Antoine Paccard, Alexandre Fruleux & Yvonne Willi

  2. Redpath Museum and Department of Biology, McGill University, 859 Sherbrooke Street West, Montreal, QC, H3A 0C4, Canada

    Antoine Paccard

Authors
  1. Antoine Paccard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandre Fruleux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yvonne Willi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antoine Paccard.

Additional information

Communicated by Christina Marie Caruso.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 67 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paccard, A., Fruleux, A. & Willi, Y. Latitudinal trait variation and responses to drought in Arabidopsis lyrata . Oecologia 175, 577–587 (2014). https://doi.org/10.1007/s00442-014-2932-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-2932-8

Keywords

Search

Navigation