Climate drives intraspecific differentiation in the expression of growth-defence trade-offs in a long-lived pine species.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
29 06 2020
Historique:
received: 28 02 2020
accepted: 01 06 2020
entrez: 1 7 2020
pubmed: 1 7 2020
medline: 16 1 2021
Statut: epublish

Résumé

Intraspecific variation in plant defences is expected to be the result of adaptive and plastic responses to environmental conditions, where trade-offs between growth and defences are thought to play a key role shaping phenotypic patterns in defensive investment. Axial resin ducts are costly defensive structures that remain imprinted in the tree rings of conifers, therefore being a valuable proxy of defensive investment along the trees' lifespan. We aimed to disentangle climate-driven adaptive clines and plastic responses to both spatial and temporal environmental variation in resin duct production, and to explore growth-defence trade-offs. To that aim, we applied dendrochronological procedures to quantify annual growth and resin duct production during a 31-year-period in a Mediterranean pine species, including trees from nine populations planted in two common gardens. Both genetic factors and plastic responses modulated annual resin duct production. However, we found no evidence of adaptive clines with climate gradients driving population differentiation. Our results revealed a marked physiological trade-off between growth and defences, where the slope of the trade-off was genetically variable and associated with climatic gradients. Our results help to enlighten the evolutionary patterns and genetic basis of defensive allocation within species, particularly revealing a key role of growth-defence trade-offs.

Identifiants

pubmed: 32601428
doi: 10.1038/s41598-020-67158-4
pii: 10.1038/s41598-020-67158-4
pmc: PMC7324371
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

10584

Références

Agrawal, A. A. Macroevolution of plant defense strategies. Trends Ecol. Evol. 22, 103–109 (2007).
pubmed: 17097760
Ehrlich, P. R. & Raven, P. H. Butterflies and plants: a study in coevolution. Evolution 18, 586–608 (1964).
Hahn, P. G. & Maron, J. L. A framework for predicting intraspecific variation in plant defense. Trends Ecol. Evol. 31, 646–656 (2016).
pubmed: 27282932
Stamp, N. Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78, 23–55 (2003).
pubmed: 12661508
Herms, D. A. & Mattson, W. J. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283–335 (1992).
Pratt, J. D. & Mooney, K. A. Clinal adaptation and adaptive plasticity in Artemisia californica: implications for the response of a foundation species to predicted climate change. Glob. Change Biol. 19, 2454–2466 (2013).
Woods, E. C., Hastings, A. P., Turley, N. E., Heard, S. B. & Agrawal, A. A. Adaptive geographical clines in the growth and defense of a native plant. Ecol. Monogr. 82, 149–168 (2012).
O’Neill, G. A., Aitken, S. N., King, J. N. & Alfaro, R. I. Geographic variation in resin canal defenses in seedlings from the Sitka spruce x white spruce introgression zone. Can. J. For. Res. 32, 390–400 (2002).
Anderson, J. T., Perera, N., Chowdhury, B. & Mitchell-Olds, T. Microgeographic patterns of genetic divergence and adaptation across environmental gradients in Boechera stricta (Brassicaceae). Am. Nat. 186, S60–S73 (2015).
pubmed: 26656218 pmcid: 4681450
Suárez-Vidal, E. et al. Drought stress modifies early effective resistance and induced chemical defences of Aleppo pine against a chewing insect herbivore. Environ. Exp. Bot. 162, 550–559 (2019).
Rigling, A., Bruhlhart, H., Braker, O. U., Forster, T. & Schweingruber, F. H. Effects of irrigation on diameter growth and vertical resin duct production in Pinus sylvestris L. on dry sites in the central Alps, Switzerland. For. Ecol. Manag. 175, 285–296 (2003).
Burghardt, K. T. Nutrient supply alters goldenrod’s induced response to herbivory. Funct. Ecol. 30, 1769–1778 (2016).
Raffa, K. F. et al. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 58, 501–517 (2008).
Thuiller, W., Lavorel, S., Araújo, M. B., Sykes, M. T. & Prentice, I. C. Climate change threats to plant diversity in Europe. Proc. Natl. Acad. Sci. USA 102, 8245–8250 (2005).
pubmed: 15919825
Kelly, A. E. & Goulden, M. L. Rapid shifts in plant distribution with recent climate change. Proc. Natl. Acad. Sci. USA 105, 11823–11826 (2008).
pubmed: 18697941
Aitken, S. N., Yeaman, S., Holliday, J. A., Wang, T. & Curtis‐McLane, S. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol. Appl. 1, 95–111 (2008).
pubmed: 25567494 pmcid: 3352395
Franks, S. J., Weber, J. J. & Aitken, S. N. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol. Appl. 7, 123–139 (2014).
pubmed: 24454552
Alberto, F. J. et al. Potential for evolutionary responses to climate change–evidence from tree populations. Glob. change biol. 19, 1645–1661 (2013).
Hoffmann, A. A. & Sgro, C. M. Climate change and evolutionary adaptation. Nature 470, 479 (2011).
pubmed: 21350480
Petit, R. J. & Hampe, A. Some evolutionary consequences of being a tree. Annu. Rev. Ecol. Evol. Syst. 37, 187–214 (2006).
Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).
pubmed: 25205436
Li, Y., Suontama, M., Burdon, R. D. & Dungey, H. S. Genotype by environment interactions in forest tree breeding: review of methodology and perspectives on research and application. Tree Genet. Genomes 13, 60 (2017).
Herms, D. A. & Mattson, W. J. Does reproduction compromise defense in woody plants? Forest Insect Guilds: Patterns of Interaction with Host Trees. US Department of Agriculture, Forest Service, General Technical Report NE-153, 35–46 (1991).
Agrawal, A. A. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25, 420–432 (2011).
Agrawal, A. A., Conner, J. K. & Rasmann, S. Tradeoffs and negative correlations in evolutionary ecology in Evolution since Darwin: the first 150 years Vol. 150 (eds. Bell, M.A., Futuyma, D. J., Eanes, W. F., & Levinton, J. S.) 243–268 (Sinauer Associates, Inc, 2010).
Coley, P. D., Bryant, J. P. & Chapin, F. S. Resource availability and plant antiherbivore defense. Science 230, 895–899 (1985).
pubmed: 17739203
Endara, M. J. & Coley, P. D. The resource availability hypothesis revisited: a meta‐analysis. Funct. Ecol. 25, 389–398 (2011).
Sampedro, L., Moreira, X. & Zas, R. Costs of constitutive and herbivore‐induced chemical defences in pine trees emerge only under low nutrient availability. J. Ecol. 99, 818–827 (2011).
Abdala‐Roberts, L., Moreira, X., Cervera, J. C. & Parra‐Tabla, V. Light availability influences growth‐defense trade‐offs in big‐leaf mahogany (Swietenia macrophylla King). Biotropica 46, 591–597 (2014).
Agrawal, A. A. A scale‐dependent framework for trade‐offs, syndromes, and specialization in organismal biology. Ecology 101, e02924 (2020).
pubmed: 31660584
Celedon, J. M. & Bohlmann, J. Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. N. Phytol. 224, 1444–1463 (2019).
Franceschi, V. R., Krokene, P., Christiansen, E. & Krekling, T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. N. Phytol. 167, 353–376 (2005).
Ferrenberg, S., Kane, J. M. & Mitton, J. B. Resin duct characteristics associated with tree resistance to bark beetles across lodgepole and limber pines. Oecologia 174, 1283–1292 (2014).
pubmed: 24305863
Kane, J. M. & Kolb, T. E. Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164, 601–609 (2010).
pubmed: 20556621
Hood, S., Sala, A., Heyerdahl, E. K. & Boutin, M. Low-severity fire increases tree defense against bark beetle attacks. Ecology 96, 1846–1855 (2015).
pubmed: 26378307
Zhao, S. & Erbilgin, N. Larger resin ducts are linked to the survival of lodgepole pine trees during mountain pine beetle outbreak. Front. Plant. Sci. 10, 1459 (2019).
pubmed: 31850006 pmcid: 6888816
Fritts, H. Tree rings and climate. (Academic Press, 1976).
Hahn, P. G., Agrawal, A. A., Sussman, K. I. & Maron, J. L. Population variation, environmental gradients, and the evolutionary ecology of plant defense against herbivory. Am. Nat. 193, 20–34 (2018).
pubmed: 30624107
Zas, R. et al. Intraspecific variation of anatomical and chemical defensive traits in Maritime pine (Pinus pinaster) as factors in susceptibility to the pinewood nematode (Bursaphelenchus xylophilus). Trees-struct. funct. 29, 663–673 (2015).
Vázquez-González, C., López-Goldar, X., Zas, R. & Sampedro, L. Neutral and climate-driven adaptive processes contribute to explain population variation in resin duct traits in a Mediterranean pine species. Front. Plant. Sci. 10, 01613 (2019).
Gaylord, M. L. et al. Drought predisposes pinon-juniper woodlands to insect attacks and mortality. N. Phytol. 198, 567–578 (2013).
Moreira, X., Zas, R., Solla, A. & Sampedro, L. Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defence constraints. Tree Physiol. 35, 112–123 (2015).
pubmed: 25595753
Lo, Y.-H., Blanco, J. A., Seely, B., Welham, C. & Kimmins, J. H. Relationships between climate and tree radial growth in interior British Columbia, Canada. For. Ecol. Manag. 259, 932–942 (2010).
Lebourgeois, F. Climatic signals in earlywood, latewood and total ring width of Corsican pine from western France. Ann. For. Sci. 57, 155–164 (2000).
Domec, J. C. & Gartner, B. L. How do water transport and water storage differ in coniferous earlywood and latewood? J. Exp. Bot. 53, 2369–2379 (2002).
pubmed: 12432029
Gindl, W., Grabner, M. & Wimmer, R. The influence of temperature on latewood lignin content in treeline Norway spruce compared with maximum density and ring width. Trees-struct. funct. 14, 409–414 (2000).
Wimmer, R. & Grabner, M. Effects of climate on vertical resin duct density and radial growth of Norway spruce Picea abies (L) Karst. Trees-struct. funct. 11, 271–276 (1997).
Wu, H. & Hu, Z. H. Comparative anatomy of resin ducts of the Pinaceae. Trees-struct. funct. 11, 135–143 (1997).
Rosner, S. & Hannrup, B. Resin canal traits relevant for constitutive resistance of Norway spruce against bark beetles: environmental and genetic variability. For. Ecol. Manag. 200, 77–87 (2004).
Westbrook, J. W. et al. Association genetics of oleoresin flow in loblolly pine: discovering genes and predicting phenotype for improved resistance to bark beetles and bioenergy potential. N. Phytol. 199, 89–100 (2013).
Saracino, A. et al. Climatic signal from Pinus leucodermis axial resin ducts: a tree-ring time series approach. Eur. J. For. Res. 136, 27–36 (2017).
Hood, S. & Sala, A. Ponderosa pine resin defenses and growth: metrics matter. Tree Physiol. 35, 1223–1235 (2015).
pubmed: 26433021
Klutsch, J. G. & Erbilgin, N. Dwarf mistletoe infection in jack pine alters growth–defense relationships. Tree Physiol. 38, 1538–1547 (2018).
pubmed: 30137634
Mason, C. J. et al. Anatomical defenses against bark beetles relate to degree of historical exposure between species and are allocated independently of chemical defenses within trees. Plant. Cell Environ. 42, 633–646 (2019).
pubmed: 30474119
Redmond, M. D., Davis, T. S., Ferrenberg, S. M. & Wion, A. P. Resource allocation trade-offs in a mast-seeding conifer: Piñon pine prioritizes reproduction over defense. AoB PLANTS 11(6), plz070 (2019).
Alía, R., Gil, L. & Pardos, J. Performance of 43 Pinus pinaster Ait. provenances on 5 locations in central Spain. Silvae Genet. 44, 75–80 (1995).
Abad Viñas, R., Caudullo, G., Oliveira, S. & de Rigo, D. Pinus pinaster in Europe: distribution, habitat, usage and threats in European Atlas of Forest Tree Species (Publi. Off. EU, Luxemburg) e012d59 (2016).
Jaramillo-Correa, J.-P. et al. Molecular proxies for climate maladaptation in a long-lived tree (Pinus pinaster Aiton, Pinaceae). Genetics 199, 793–807 (2015).
pubmed: 25549630
Bucci, G. et al. Range‐wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Mol. Ecol. 16, 2137–2153 (2007).
pubmed: 17498237
Arrabal, C., Cortijo, M., de Simón, B. F., Vallejo, M. C. G. & Cadahía, E. Differentiation among five Spanish Pinus pinaster provenances based on its oleoresin terpenic composition. Biochem. Syst. Ecol. 33, 1007–1016 (2005).
Correia, I. et al. Variations in growth, survival and carbon isotope composition (δ13C) among Pinus pinaster populations of different geographic origins. Tree Physiol. 28, 1545–1552 (2008).
pubmed: 18708336
Santos-del-Blanco, L., Climent, J., González-Martínez, S. & Pannell, J. Genetic differentiation for size at first reproduction through male versus female functions in the widespread Mediterranean tree Pinus pinaster. Ann. Bot. 110, 1449–1460 (2012).
pubmed: 23002272 pmcid: 3489151
Hengl, T. et al. SoilGrids1km—global soil information based on automated mapping. PLoS One 9, e105992 (2014).
pubmed: 25171179 pmcid: 4149475
Alía, R., Serrano, J. M. & Denis, J. Ensayos de procedencias de Pinus pinaster Ait. en el centro de España: resultados a la edad de 32 años. Invest. Agrar. Sist. Recur. For. 10, 333–354 (2001).
Holmes, R. L. Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bul. 43, 69–78 (1983).
Biondi, F. & Qeadan, F. A theory-driven approach to tree-ring standardization: defining the biological trend from expected basal area increment. Tree-Ring Res. 64, 81–97 (2008).
Gonzalo, J. Phytoclimatic analysis of the Spanish Peninsula: update and geostatistical analysis, PhD Thesis, University of Valladolid, Palencia, Spain, (2008).
Mitchell, T. D. & Jones, P. D. An improved method of constructing a database of monthly climate observations and associated high resolution grids. Int. J. Climatol. 25, 693–712 (2005).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82 (2017).
Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).
Wickham, H. ggplot2: elegant graphics for data analysis. (Springer, 2016).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2014).

Auteurs

Carla Vázquez-González (C)

Misión Biológica de Galicia - Consejo Superior de Investigaciones Científicas (MBG-CSIC), 36143, Pontevedra, Spain. cvazquez@mbg.csic.es.

Luis Sampedro (L)

Misión Biológica de Galicia - Consejo Superior de Investigaciones Científicas (MBG-CSIC), 36143, Pontevedra, Spain.

Vicente Rozas (V)

iuFOR-EiFAB, Campus Duques de Soria, Universidad de Valladolid, 42004, Soria, Spain.
Laboratorio de Dendrocronología y Cambio Global, Facultad de Ciencias Forestales y Recursos Naturales, Universidad Austral de Chile, Valdivia, Chile.

Rafael Zas (R)

Misión Biológica de Galicia - Consejo Superior de Investigaciones Científicas (MBG-CSIC), 36143, Pontevedra, Spain.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Animals Lung India Sheep Transcriptome
Eimeria tenella Animals Antigens, Protozoan Chickens Genetic Variation

Classifications MeSH