Abstract
Global warming has increased the stress conditions faced by natural populations of forest species. Genetic variation (GV) and phenotypic plasticity (PP) of adaptive traits are the main mechanisms by which these species survive the in situ effects of environmental fluctuation including a higher frequency of stressful events. This study evaluated the level of GV and PP in annual shoot growth and bud phenology traits such as bud flush and bud set date in 44 families of Pinus pseudostrobus from central Mexico established in an open-pollinated progeny trial replicated at two sites with different soil and climate conditions. Results showed wide GV in seasonal shoot growth pattern and strong genetic control in bud phenology traits. Shoot growth, particularly activation and formation of terminal bud, and shoot growth during wintertime, showed an adaptive relationship with climate conditions of origin site of families, particularly with moisture availability and aridity index. Despite the significant effect of test site on shoot growth, families exhibited consistent performance across sites for most traits, except for wintertime shoot growth (WSG) which showed a significant genotype x environment interaction. PP in WSG showed moderate genetic control and positive relationship with productivity (total height). The adaptive value of the GV and PP of shoot growth traits could allow P. pseudostrobus populations to mitigate the negative impacts of environmental fluctuations associated with global warming and provide competitive advantages in productivity for domestication purposes.
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Aitken SN, Bemmels JB (2016) Time to get moving: assisted gene flow of forest trees. Evol Appl 9:271–290. https://doi.org/10.1111/eva.12293
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Ecol Manag 259:660–684. https://doi.org/10.1016/j.foreco.2009.09.001
Barros FDV, Goulart MF, Sá Telles SB, Lovato MB, Valladares F, Lemos-Filho JD (2012) Phenotypic plasticity to light of two congeneric trees from contrasting habitats: Brazilian Atlantic Forest versus Cerrado (savanna). Plant Biol 14:208–215. https://doi.org/10.1111/j.1438-8677.2011.00474.x
Baythavong BS (2011) Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments. Am Nat 178:75–87. https://doi.org/10.1086/660281
Chambel MR, Climent J, Alía R (2007) Divergence among species and populations of Mediterranean pines in biomass allocation of seedlings grown under two watering regimes. Ann Sci 64:87–97. https://doi.org/10.1051/forest:2006092
Chevin LM, Lande R (2011) Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J Evol Biol 24:1462–1476. https://doi.org/10.1111/j.1420-9101.2011.02279.x
Codesido V, Fernández-López J (2009) Genetic variation in seasonal growth patterns in radiata pine in Galicia (northern Spain). Ecol Manag 257:518–526. https://doi.org/10.1016/j.foreco.2008.09.026
Cook BI, Mankin JS, Anchukaitis KJ (2018) Climate change and drought: from past to future. Curr Clim Change Rep 4:164–179. https://doi.org/10.1007/s40641-018-0093-2
Cooke JE, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728. https://doi.org/10.1111/j.1365-3040.2012.02552.x
Cooper HF, Grady KC, Cowan JA, Best RJ, Allan GJ, Whitham TG (2019) Genotypic variation in phenological plasticity: reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost. Global Change Biol 25:187–200. https://doi.org/10.1111/gcb.14494
De Kort H, Panis B, Helsen K, Douzet R, Janssens SB, Honnay O (2020) Pre-adaptation to climate change through topography‐driven phenotypic plasticity. J Ecol 108:1465–1474. https://doi.org/10.1111/1365-2745.13365
Dickerson GE (1969) Techniques for research in quantitative animal genetics. In: Chapman AB (ed) Techniques and procedures in animal science research. American Society of Animal Science, Albany, pp 36–79
Ehrlén J, Van Groenendael JM (1998) The trade-off between dispersability and longevity‐an important aspect of plant species diversity. Appl Veg Sci 1:29–36. https://doi.org/10.2307/1479083
Falconer DS, Mackay TFC (1996) Introduction to quantitative Genetics. Longmans Green, Harlow
Farjon A (2010) A handbook of the world’s conifers. Brill, Leiden, pp 742–745
Fichot R, Barigah TS, Chamaillard S, Le Thiec D, Laurans F, Cochard H, Brignolas F (2010) Common trade-offs between xylem resistance to cavitation and other physiological traits do not hold among unrelated Populus deltoides× Populus nigra hybrids. Plant Cell Environ 33:1553–1568. https://doi.org/10.1111/j.1365-3040.2010.02164.x
Franks SJ, Weber JJ, Aitken SN (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol Appl 7:123–139. https://doi.org/10.1111/eva.12112
Fry DJ, Phillips IDJ (1977) Photosynthesis of conifers in relation to annual growth cycles and dry matter production: II. Seasonal photosynthetic capacity and mesophyll ultrastructure in Abies grandis, Picea sitchensis, Tsuga heterophylla and Larix leptolepis growing in SW England. Physiol Plant 40:300–306. https://doi.org/10.1111/j.1399-3054.1977.tb04077.x
Gazol A, Camarero JJ, Anderegg WRL, Vicente-Serrano SM (2017) Impacts of droughts on the growth resilience of Northern Hemisphere forests. Global Ecol Biogeogr 26:166–176. https://doi.org/10.1111/geb.12526
GBIF.org (2023) GBIF occurrence download. https://doi.org/10.15468/dl.7rw4es
Gernandt DS, Pérez-de la Rosa JA (2014) Biodiversity of Pinophyta (conifers) in Mexico. Rev Mex Biodivers 85:126–133. https://doi.org/10.7550/rmb.32195
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x
Gianoli E, González-Teuber M (2005) Environmental heterogeneity and population differentiation in plasticity to drought in Convolvulus chilensis (Convolvulaceae). Evol Ecol 19:603–613. https://doi.org/10.1007/s10682-005-2220-5
Gómez-Pineda E, Hammond WM, Trejo-Ramirez O, Gil-Fernández M, Allen CD, Blanco-García A, Sáenz-Romero C (2022) Drought years promote bark beetle outbreaks in Mexican forests of Abies religiosa and Pinus pseudostrobus. Ecol Manage 505:119944. https://doi.org/10.1016/j.foreco.2021.119944
Grenier S, Barre P, Litrico I (2016) Phenotypic plasticity and selection: nonexclusive mechanisms of adaptation. Scientifica 2016:1–9. https://doi.org/10.1155/2016/7021701
Harrington C, Ford K, Clair S B (2016) Phenology of pacific northwest tree species. Tree Planters’ Notes 59:76–85. https://www.fs.usda.gov/pnw/pubs/journals/pnw_2016_harrington001.pdf
Hendry AP (2016) Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J Hered 107:25–41. https://doi.org/10.1093/jhered/esv060
Hof C, Levinsky I, Araujo MB, Rahbek C (2011) Rethinking species’ ability to cope with rapid climate change. Global Change Biol 17:2987–2990. https://doi.org/10.1111/j.1365-2486.2011.02418.x
Hoffmann A, Sgrò C (2011) Climate change and evolutionary adaptation. Nature 470:479–485. https://doi.org/10.1038/nature09670
Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204. https://doi.org/10.1093/genetics/130.1.195
IPCC (Intergovernmental Panel on Climate Change) (2022) Sixth assessment report: impacts, adaptations, vulnerabilities. https://www.ipcc.ch/report/ar6/wg2
Jezkova T, Wiens JJ (2016) Rates of change in climatic niches in plant and animal populations are much slower than projected climate change. Proc R Soc Ser B Biol Sci 283:2016–2104. https://doi.org/10.1098/rspb.2016.2104
Jump AS, Hunt JM, Martínez-Izquierdo JA, Peñuelas J (2006) Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Mol Ecol 15:3469–3480. https://doi.org/10.1111/j.1365-294X.2006.03027.x
Kaya Z, Campbell RK, Adams WT (1989) Correlated responses of height increment and components of increment in 2-year-old Douglas-fir. Can J Res 19:1124–1130. https://doi.org/10.1139/x89-170
Kerr KL, Meinzer FC, McCulloh KA, Woodruff DR, Marias DE (2015) Expression of functional traits during seedling establishment in two populations of Pinus ponderosa from contrasting climates. Tree Physiol 35:535–548. https://doi.org/10.1093/treephys/tpv034
Körner C, Basler D (2010) Phenology under global warming. Science 327:1461–1462. https://doi.org/10.1126/science.1186473
Kreyling J, Puechmaille SJ, Malyshev AV, Valladares F (2019) Phenotypic plasticity closely linked to climate at origin and resulting in increased mortality under warming and frost stress in a common grass. Ecol Evol 9:1344–1352. https://doi.org/10.1002/ece3.4848
Lamy JB, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H, Plomion C (2014) Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytol 201:874–886. https://doi.org/10.1111/nph.12556
Li P, Adams WT (1993) Genetic control of bud phenology in pole-size trees and seedlings of coastal Douglas-fir. Can J Res 23:1043–1051. https://doi.org/10.1139/x93-133
López-Upton J (2002) Pinus pseudostrobus. In: Vozzo J (ed) Tropical tree seed Manual. Agriculture Handbook 721. USDA Forest Service, Washington, pp 636–638
Luquez V, Hall D, Albrectsen BR, Karlsson J, Ingvarsson P, Jansson S (2008) Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genet Genomes 4:279–292. https://doi.org/10.1007/s11295-007-0108-y
McKown AD, Guy RD, Klápště J, Geraldes A, Friedmann M, Cronk QC, Douglas CJ (2014) Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytol 201:1263–1276. https://doi.org/10.1111/nph.12601
Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14. https://doi.org/10.1111/eva.12137
Mihai G, Mirancea I, Birsan MV, Dumitrescu A (2018) Patterns of genetic variation in bud flushing of Abies alba populations. iForest 11:284–290. https://doi.org/10.3832/ifor2314-011
Munguía-Rosas MA (2022) Domestication reduces phenotypic plasticity in chaya (Cnidoscolus aconitifolius (Mill.) IM Johnst). Bot Sci 100:93–106. https://doi.org/10.17129/botsci.2879
Nicotra AB, Hermes JP, Jones CS, Schlichting CD (2007) Geographic variation and plasticity to water and nutrients in Pelargonium australe. New Phytol 176:136–149. https://doi.org/10.1111/j.1469-8137.2007.02157.x
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692. https://doi.org/10.1016/j.tplants.2010.09.008
Oddou-Muratorio S, Davi H (2014) Simulating local adaptation to climate of forest trees with a Physio‐Demo‐Genetics model. Evol Appl 7:453–467. https://doi.org/10.1111/eva.12143
Oleksyn J, Modrzýnski J, Tjoelker MG, Zytkowiak R, Reich PB, Karolewski P (1998) Growth and physiology of Picea abies populations from elevational transects: common garden evidence for altitudinal ecotypes and cold adaptation. Funct Ecol 12:573–590. https://doi.org/10.1046/j.1365-2435.1998.00236.x
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. https://doi.org/10.1038/nature01286
Pellissier L, Albouy C, Bascompte J, Farwig N, Graham C, Loreau M, Gravel D (2018) Comparing species interaction networks along environmental gradients. Biol Rev 93:785–800. https://doi.org/10.1111/brv.12366
Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214. https://doi.org/10.1146/annurev.ecolsys.37.091305.110215
Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367. https://doi.org/10.1242/jeb.02070
Pires MV, de Castro EM, de Freitas BSM, Lira JMS, Magalhães PC, Pereira MP (2020) Yield-related phenotypic traits of drought resistant maize genotypes. Environ Exp Bot 171:103962. https://doi.org/10.1016/j.envexpbot.2019.103962
Quesada T, Parisi LM, Huber DA, Gezan SA, Martin TA, Davis JM, Peter GF (2017) Genetic control of growth and shoot phenology in juvenile loblolly pine (Pinus taeda L.) clonal trials. Tree Genet Genomes 13:1–15. https://doi.org/10.1007/s11295-017-1143-y
Rehfeldt GE, Ferguson DE, Crookston NL (2009) Aspen, climate, and sudden decline in western USA. Ecol Manag 258:2353–2364. https://doi.org/10.1016/j.foreco.2009.06.005
Rehfeldt GE, Leites LP, St Clair JB, Jaquish BC, Sáenz-Romero C, López-Upton J, Joyce DG (2014) Comparative genetic responses to climate in the varieties of Pinus ponderosa and Pseudotsuga menziesii: Clines in growth potential. Ecol Manag 324:138–146. https://doi.org/10.1016/j.foreco.2014.02.041
Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301. https://doi.org/10.1111/1365-2745.12211
Rousi M, Heinonen J (2007) Temperature sum accumulation effects on within-population variation and long-term trends in date of bud burst of European white birch (Betula pendula). Tree Physiol 27:1019–1025. https://doi.org/10.1093/treephys/27.7.1019
Rweyongeza DM, Yeh FC, Dhir NK (2010) Genetic parameters for bud flushing and growth characteristics of white spruce seedlings. Silvae Genet 59:151–158. https://doi.org/10.1515/sg-2010-0018
Salmela MJ, Cavers S, Cottrell JE, Iason GR, Ennos RA (2013) Spring phenology shows genetic variation among and within populations in seedlings of scots pine (Pinus sylvestris L.) in the Scottish highlands. Plant Ecol divers. 6:523–536. https://doi.org/10.1080/17550874.2013.795627
Sampaio T, Branco M, Guichoux E, Petit RJ, Pereira JS, Varela MC, Almeida MH (2016) Does the geography of cork oak origin influence budburst and leaf pest damage? Ecol Manag 373:33–43. https://doi.org/10.1016/j.foreco.2016.04.019
Sandoval-García R, Gonzalez-Cubas R, Bautista-Cruz A (2020) Ecological association of Pinus pseudostrobus (Pinaceae) in response to biogeographical variations in Central-Southern of Mexico. Acta Bot Mex 127:e1627. https://doi.org/10.21829/abm127.2020.1627
SAS Institute Inc (2014) SAS® OnDemand for academics: user’s guide. SAS Institute Inc, Cary. https://support.sas.com/bookstore
Schlichting CD, Pigliucci M (1993) Control of phenotypic plasticity via regulatory genes. Am Nat 142:366–370. https://doi.org/10.1086/285543
Singh A, Roy S (2017) High altitude population of Arabidopsis thaliana is more plastic and adaptive under common garden than controlled condition. BMC Ecol 17:1–16. https://doi.org/10.1186/s12898-017-0149-5
Solé-Medina A, Robledo‐Arnuncio JJ, Ramírez‐Valiente JA (2022) Multi‐trait genetic variation in resource‐use strategies and phenotypic plasticity correlates with local climate across the range of a Mediterranean oak (Quercus faginea). New Phytol 234:462–478. https://doi.org/10.1111/nph.17968
Song Y, Sass-Klaassen U, Sterck F, Goudzwaard L, Akhmetzyanov L, Poorter L (2021) Growth of 19 conifer species is highly sensitive to winter warming, spring frost and summer drought. Ann Bot 128:545–557. https://doi.org/10.1093/aob/mcab090
Squillace AE (1974) Average genetic correlations among offspring from open pollinated forest trees. Silvae Genet 23:149–156
Thompson JD (1991) Phenotypic plasticity as a component of evolutionary change. Trends Ecol Evol 6:246–249. https://doi.org/10.1016/0169-5347(91)90070-E
Thuiller W, Lavorel S, Sykes MT, Araújo MB (2006) Using niche-based modelling to assess the impact of climate change on tree functional diversity in Europe. Divers Distrib 12:49–60. https://doi.org/10.1111/j.1366-9516.2006.00216.x
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116. https://doi.org/10.1111/j.1365-2745.2006.01176.x
Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217. https://doi.org/10.1016/S0169-5347(00)89061-8
Vitasse Y, Delzon S, Dufrêne E, Pontailler JY, Louvet JM, Kremer A, Michalet R (2009) Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses? Agric Meteorol 149:735–744. https://doi.org/10.1016/j.agrformet.2008.10.019
Vitasse Y, Hoch G, Randin CF, Lenz A, Kollas C, Scheepens JF, Körner C (2013) Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171:663–678. https://doi.org/10.1007/s00442-012-2580-9
Viveros-Viveros H, Sáenz-Romero C, Vargas-Hernández JJ, López-Upton J (2006) Pinus pseudostrobus provenance variation tested in two sites in Michoacán, México. Rev Fitotec Mex 29:121–121. https://doi.org/10.35196/rfm.2006.2.121
Viveros-Viveros H, Tapia-Oivares BL, Sáenz-Romero C (2014) Pinus Pseudostrobus Lindl. Isoenzimatic variation along an altitudinal gradient in Michoacán. Mexico Agrociencia 48:713–723. https://agrociencia-colpos.org/index.php/agrociencia/article/view/1114/1114
Vizcaíno-Palomar N, Fady B, Alía R, Raffin A, Mutke S, Garzón MB (2019) Patterns of phenotypic plasticity among populations of three Mediterranean pine species and implications for evolutionary responses to climate change. bioRxiv 716084. https://doi.org/10.1101/716084
Voltas J, Chambel MR, Prada MA, Ferrio JP (2008) Climate-related variability in carbon and oxygen stable isotopes among populations of Aleppo pine grown in common-garden tests. Trees 22:759–769. https://doi.org/10.1007/s00468-008-0236-5
Wang T, Hamann A, Spittlehouse D, Carroll C (2016) Locally downscaled and spatially customizable climate data for historical and future periods for North America. PLoS ONE 11(6):e0156720. https://doi.org/10.1371/journal.pone.0156720
White TL, Hodge GR (1989) Predicting breeding values with applications in forest tree improvement. Kluwer Academic, London, p 368. https://doi.org/10.1007/978-94-015-7833-2
Yamada Y (1962) Genotype by environment interaction and genetic correlation of the same trait under different environments. Jpn J Hum Genet 37:498–509. https://doi.org/10.1266/jjg.37.498
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S.E.A., J.J.V.H. and J.L.U set up the field experiment, S.E.A and J.J.V.H. did the statistical analysis and wrote the first draft of the manuscript. J.L.U, F.G.C., M.J.C. and N.C.H. provided valuable advice on the statistical analysis and made substantial contributions to the interpretation of data and discussion of results. All authors reviewed the final version of manuscript.
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Escobar-Alonso, S., Vargas-Hernández, J.J., López-Upton, J. et al. Genetic variation and phenotypic plasticity in the seasonal shoot growth pattern of Pinus pseudostrobus. New Forests (2024). https://doi.org/10.1007/s11056-024-10040-2
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DOI: https://doi.org/10.1007/s11056-024-10040-2