Environment-dependent microevolution in a Mediterranean pine (Pinus pinaster Aiton)

BMC Evolutionary Biology

Santiago C González-Martínez⁴  José Climent³  Eduardo Notivol¹  Regina Chambel²  Ricardo Alía³ 

[1]Unit of Forest Resources, CITA. Carr. Montañana s/n, Zaragoza, 50059, Spain

[2]Department of Forest Ecology and Genetics, INIA-Forest Research Centre (CIFOR), Avda. A Coruña km 7.5, Madrid, Spain

[3]Sustainable Forest Management Research Institute, University of Valladolid-INIA, Madrid, Spain

[4]Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

关键词: Mediterranean forest;    Phenotypic directional selection;    Selection gradients;    Response to selection;    Adaptive traits;   

Others  :  1117939
DOI  :  10.1186/s12862-014-0200-5

 received in 2014-06-06, accepted in 2014-09-08,  发布年份 2014

【 摘 要 】

Background

A central question for understanding the evolutionary responses of plant species to rapidly changing environments is the assessment of their potential for short-term (in one or a few generations) genetic change. In our study, we consider the case of Pinus pinaster Aiton (maritime pine), a widespread Mediterranean tree, and (i) test, under different experimental conditions (growth chamber and semi-natural), whether higher recruitment in the wild from the most successful mothers is due to better performance of their offspring; and (ii) evaluate genetic change in quantitative traits across generations at two different life stages (mature trees and seedlings) that are known to be under strong selection pressure in forest trees.

Results

Genetic control was high for most traits (h² = 0.137-0.876) under the milder conditions of the growth chamber, but only for ontogenetic change (0.276), total height (0.415) and survival (0.719) under the more stressful semi-natural conditions. Significant phenotypic selection gradients were found in mature trees for traits related to seed quality (germination rate and number of empty seeds). Moreover, female relative reproductive success was significantly correlated with offspring performance for specific leaf area (SLA) in the growth chamber experiment, and stem mass fraction (SMF) in the experiment under semi-natural conditions, two adaptive traits related to abiotic stress-response in pines. Selection gradients based on genetic covariance of seedling traits and responses to selection at this stage involved traits related to biomass allocation (SMF) and growth (as decomposed by a Gompertz model) or delayed ontogenetic change, depending also on the testing environment.

Conclusions

Despite the evidence of microevolutionary change in adaptive traits in maritime pine, directional or disruptive changes are difficult to predict due to variable selection at different life stages and environments. At mature-tree stages, higher female effective reproductive success can be explained by differences in their production of offspring (due to seed quality) and, to a lesser extent, by seemingly better adapted seedlings. Selection gradients and responses to selection for seedlings also differed across experimental conditions. The distinct processes involved at the two life stages (mature trees or seedlings) together with environment-specific responses advice caution when predicting likely evolutionary responses to environmental change in Mediterranean forest trees.

【 授权许可】

   
2014 Alia et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S: Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 2008, 1:95-111.
• [2]Petit RJ, Hu FS, Dick CW: Forests of the past: a window to future changes. Science 2008, 320:1450-1452.
• [3]Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, Leroy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC: A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 2006, 7:510-523.
• [4]Hamrick JL: Response of forest trees to global environmental changes. For Ecol Manage 2004, 197:323-335.
• [5]Price GR: Selection and covariance. Nature 1970, 227:520-521.
• [6]Lande R, Arnold SJ: The measurement of selection on correlated characters. Evolution 1983, 37:1210-1226.
• [7]Wright JW, Meagher TR: Selection on floral characters of natural Spanish populations of Silene latifolia. J Evol Biol 2004, 17:382-395.
• [8]Morgan MT, Conner JK: Using genetic markers to directly estimate male selection gradients. Evolution 2001, 55:272-281.
• [9]Rausher MD: The measurement of selection of quantitative traits: biases due to environmental covariances between traits and fitness. Evolution 1992, 46:616-626.
• [10]Houle D: Comparing evolvability and variability of quantitative traits. Genetics 1992, 130:195-204.
• [11]Kruuk LEB: Estimating genetic parameters in natural populations using the “animal model”. Philos Trans R Soc Lond B 2004, 359:873-890.
• [12]Hadfield JD, Wilson AJ, Garant D, Sheldon BC, Kruuk LEB: The misuse of BLUP in ecology and evolution. Am Nat 2010, 175:116-125.
• [13]Campbell DR: Effects of floral traits on sequential components of fitnes in Ipomopsis aggregata. Am Nat 1991, 137:713-737.
• [14]Oddou-Muratorio S, Klein EK, Austerlitz F: Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. II. Pollen dispersal and heterogeneity in mating success inferred from parent-offspring analysis. Mol Ecol 2005, 14:4441-4452.
• [15]Castro J: Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytol 1999, 144:153-161.
• [16]Naito Y, Konuma A, Iwata H, Suyama Y, Seiwa K, Okuda T, Lee SL, Muhammad N, Tsumura Y: Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae). J Plant Res 2005, 118:423-430.
• [17]Kärkkäinen K, Savolainen O, Koski V: Why do plants abort so many developing seeds: bad offspring or bad maternal genotypes? Evol Ecol 1999, 13:305-317.
• [18]Steven DDE, Wright SJ: Consequences of variable reproduction for seedling recruitment in three neotropical tree species. Ecology 2011, 83:2315-2327.
• [19]Kolb A: Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. J Ecol 2005, 93:1226-1237.
• [20]Nathan R, Casagrandi R: A simple mechanistic model of seed dispersal, predation and plant establishment: Janzen-Connell and beyond. J Ecol 2004, 92:733-746.
• [21]Leck MA, Parker VT, Simpson RL: Seedling Ecology and Evolution. Cambridge University Press, Cambridge; 2008.
• [22]Miguel I, González-Martínez SC, Alia R, Gil LA: Growth phenology and mating system of maritime pine (Pinus pinaster Aiton) in central Spain. Inv Agrar Sist y Rec For 2002, 11:193-204.
• [23]Castro J, Zamora R, Hodar JA, Gomez JM: Seedling establishment of a boreal tree species (Pinus sylvestris) at its southernmost distribution limit: consequences of being in a marginal Mediterranean habitat. J Ecol 2004, 92:266-277.
• [24]Petit RJ, Hampe A: Some evolutionary consequences of being a tree. Ann Rev Ecol Evol Syst 2006, 37:187-214.
• [25]González-Martínez SC, Gerber S, Cervera MT, Martínez-Zapater JM, Alia R, Gil LA: Selfing and sibship structure in a two-cohort stand of maritime pine (Pinus pinaster Ait.) using nuclear SSR markers. Ann For Sci 2003, 60:115-121.
• [26]González-Martínez SC, Burczyk J, Nathan R, Nanos N, Gil LA, Alia R: Effective gene dispersal and female reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton). Mol Ecol 2006, 15:4577-4588.
• [27]Lascoux DM, Kremer A, Dormling I: Growth and phenology of 1-year-old maritime pine (Pinus pinaster) seedlings under continuous light - implications for early selection. Can J For Res 1993, 23:1325-1336.
• [28]Jonsson A, Eriksson G, Ye ZH, Yeh FC: A retrospective early test of Pinus sylvestris seedlings grown at wide and dense spacing. Can J For Res 2000, 30:1443-1452.
• [29]Notivol E, Garcia-Gil MR, Alia R, Savolainen O: Genetic variation of growth rhythm traits in the limits of a latitudinal cline in Scots pine. Can J For Res 2007, 37:540-551.
• [30]De-Lucas AI, Robledo-Arnuncio JJ, Hidalgo E, González-Martínez SC: Mating system and pollen gene flow in Mediterranean maritime pine. Heredity 2008, 100:390-399.
• [31]Meagher TR, Thompson EA: The relationship between single parent and parent pair genetic likelihoods in genealogy reconstruction. Theor Popul Biol 1986, 29:87-106.
• [32]Gerber S, Mariette S, Streiff R, Bodénès C, Kremer A: Comparison of microsatellites and amplified fragment length polymorphism markers for parentage analysis. Mol Ecol 2000, 9:1037-1048.
• [33]González-Martínez SC, Gerber S, Cervera MT, Martínez-Zapater J, Gil LA, Alia R, Martínez-Zapater M: Seed gene flow and fine-scale structure in a Mediterranean pine (Pinus pinaster Ait.) using nuclear microsatellite markers. Theor Appl Genet 2002, 104:1290-1297.
• [34]Devlin B, Roeder K, Ellstrand NC: Fractional paternity assignment: theoretical development and comparison to other methods. Theor Appl Genet 1988, 76:369-380.
• [35]Climent J, Chambel MR, Pardos M, Lario F, Villar-Salvador P: Biomass allocation and foliage heteroblasty in hard pine species respond differentially to reduction in rooting volume. Eur J For Res 2011, 130:841-850.
• [36]Poorter H, Nagel O: The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review.Aust J Plant Physiol 2000, 27:595–607.
• [37]Cregg BM, Zhang JW: Physiology and morphology of Pinus sylvestris seedlings from diverse sources under cyclic drought stress. For Ecol Manage 2001, 154:131-139.
• [38]Nguyen-Queyrens A, Ferhi A, Loustau D, Guehl J-M: Within-ring δ13C spatial variability and interannual variations in wood cellulose of two contrasting provenances ofPinus pinaster.Can J For Res 1998, 28:766–773.
• [39]Fernández M, Gil LA, Pardos JA: Response of Pinus pinaster Ait. provenances at early age to water supply. I. Water relation parameters. Ann For Sci 1999, 56:179-187.
• [40]Climent J, Silva FCE, Chambel MR, Pardos M, Almeida MH: Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting ecological niches. Ann For Sci 2009, 66:407-414.
• [41]Harfouche A: Retrospective early test for adult vigor of Pinus pinaster families grown under two water regimes. Implications for early selection. Ann For Sci 2003, 60:539-547.
• [42]Chambel MR, Climent J, Alia R: Divergence among species and populations of Mediterranean pines in biomass allocation of seedlings grown under two watering regimes. Ann For Sci 2007, 64:87-97.
• [43]Aranda I, Alia R, Ortega U, Dantas ÂK, Majada J: Intra-specific variability in biomass partitioning and carbon isotopic discrimination under moderate drought stress in seedlings from four Pinus pinaster populations. Tree Genet Genomes 2010, 6:169-178.
• [44]Sanchez-Gomez D, Majada J, Alia R, Feito I, Aranda I: Intraspecific variation in growth and allocation patterns in seedlings of Pinus pinaster Ait. submitted to contrasting watering regimes: can water availability explain regional variation? Ann For Sci 2010, 67:505-513.
• [45]Gilmour AR, Gogel BJ, Cullis BR, Thompson R: ASReml User Guide Release 4.0. Hemel Hempstead, HP1. 1ES. VSN International Ltd, UK; 2012.
• [46]Lynch M, Walsh B: Genetics and Analysis of Quantitative Traits. Sinauer Assoc, Massachusetts; 1998.
• [47]Fahrmeir L, Tutz G: Multivariate Statistical Modelling Based on Generalized Linear Models. Springer-Verlag, New York; 1994.
• [48]Costa e Silva J, Kerr RJ: Accounting for competition in genetic analysis, with particular emphasis on forest genetic trials. Tree Genet Genomes 2013, 9:1-17.
• [49]Grant PR, Grant BR: Predicting microevolutionary responses to directional selection on heritable variation. Evolution 1995, 49:241-251.
• [50]Climent J, Chambel MR, Lopez R, Mutke S, Alia R, Gil LA: Population divergence for heteroblasty in the Canary Island pine (Pinus canariensis, Pinaceae). Am J Bot 2006, 93:840-848.
• [51]Benito-Garzón M, Alia R, Robson TM, Zavala MA: Intra-specific variability and plasticity influence potential tree species. Glob Ecol Biogeogr 2011, 20:766-788.
• [52]Chevin L-M, Lande R, Mace GM: Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 2010, 8:e1000357.
• [53]Valladares F, Gianoli E, Gomez JM: Ecological limits to plant phenotypic plasticity. New Phytol 2007, 176:749-763.
• [54]Chevin L-M, Collins S, Lefèvre F: Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Funct Ecol 2013, 27:967-979.
• [55]Sánchez-Gómez D, Valladares F, Zavala MA: Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytol 2006, 170:795-806.
• [56]Gaspar MJ, Velasco T, Feito I, Alía R, Majada J: Genetic variation of drought tolerance in Pinus pinaster at three hierarchical levels: a comparison of induced osmotic stress and field testing. PLoS One 2013, 8:e79094.
• [57]Obeso JR: A hierarchical perspective in allocation to reproduction from whole plant to fruit and seed level. Perspect Plant Ecol Evol Syst 2004, 6:217-225.
• [58]Bateman AJ: Intrasexual selection in Drosophila. Heredity 1948, 2:349-368.
• [59]Durel CE, Bertin P, Kremer A: Relationship between inbreeding depression and inbreeding coefficient in maritime pine (Pinus pinaster). Theor Appl Genet 1996, 92:347-356.
• [60]De-Lucas AI, González-Martínez SC, Vendramin GG, Hidalgo E, Heuertz M: Spatial genetic structure in continuous and fragmented populations of Pinus pinaster Aiton. Mol Ecol 2009, 18:4564-4576.
• [61]Reich PB, Ellsworth DS, Walters MB: Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 1998, 12:948-958.
• [62]Steinger T, Roy BA, Stanton ML: Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis. J Evol Biol 2003, 16:313-323.
• [63]Galmes J, Cifre J, Medrano H, Flexas J, Galmés J: Modulation of relative growth rate and its components by water stress in Mediterranean species with different growth forms. Oecologia 2005, 145:21-31.
• [64]Agrawal AA, Erwin AC, Cook SC: Natural selection on and predicted responses of ecophysiological traits of swamp milkweed (Asclepias incarnata). J Ecol 2008, 96:536-542.
• [65]Schmid B, Dolt C: Effects of maternal and paternal environment and genotype on offspring phenotype in Solidago altissima L. Evolution 1994, 48:1525-1549.
• [66]Sgrò CM, Hoffmann AA: Genetic correlations, tradeoffs and environmental variation. Heredity 2004, 93:241-248.
• [67]Bell G: Fluctuating selection: the perpetual renewal of adaptation in variable environments. Phil Trans R Soc Lond B 2010, 365:87-97.
• [68]Nathan R, Ne’eman G: Spatiotemporal dynamics of recruitment in Aleppo pine (Pinus halepensis Miller). Plant Ecol 2004, 171:123-137.