Phenotypic plasticity is stronger than adaptative differentiation among Mediterranean stone pine provenances

Sven Mutke, Javier Gordo, M Regina Chambel, M. Aránzazu Prada, Daniel Álvarez, Salustiano Iglesias, Luis Gil


The Mediterranean stone pine, Pinus pinea L., seems to be well adapted to the different climate zones of its distribution range that spans four thousand kilometres along the Northern shore of the Mediterranean Sea. But recent molecular studies revealed it to be extremely genetically depauperate for a widespread tree. In this context, a provenances trial should elucidate whether any differentiation in adaptative traits can be identified between 34 accessions covering its natural range. The presence of strong spatial autocorrelations throughout four test sites required iterative nearest-neighbours adjustments in their statistical analysis. No significant differences in survival or ontogeny were found between accessions, while height growth was slightly though significantly more vigorous in northern or inland provenances. But these differences were masked by a common, stable reaction norm in dependence on site and microsite. On the other hand, its strong developmental plasticity allows the stone pine to delay the heteroblastic phase change in order to survive in unfavourable conditions, a clear advantage in the limiting and unpredictable environments of Mediterranean ecosystems.


Pinus pinea, spatial adjustment

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Ammannati R., 1989. Effetti dell'autoimpollinazione sulla crescita in altezza in Pinus pinea L. Monti e Boschi 39, 50-56.

Anselin L., 1995. Local Indicators of Spatial Association-LISA. Geog Anal 27, 93-115.

Archaux F., Wolters V., 2006. Impact of summer drought on forest biodiversity: what do we know? Ann For Sci 63, 645-652. doi: 10.1051/forest:2006041.

Bartlett M.S., 1978. Nearest neighbour models in the analysis of field experiments. J R Statist Soc B 40, 147-174.

Besnard G., Achere V., Jeandroz S., Johnsen Ø., Faivre Rampant P., Baumann R., Müllerstarck G., Skrøppa T., Fauvre J.M., 2008. Does maternal environmental condition during reproductive development induce genotypic selection in Picea abies? Ann For Sci 65, article 109. doi: 10.1051/forest:2007081.

Boots B., 2002. Local measures of spatial association. Ecoscience 9, 168-176.

Boys J., Cherry M., Dayanandan S., 2005. Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa, Pinaceae). Am J Bot 92(5), 833-841. PMid:21652464

Calama R., Cañadas N., Montero G., 2003. Interregional variability in site index models for even-aged stands of stone pine (Pinus pinea L.) in Spain. Ann For Sci 60, 259-269. doi: 10.1051/forest:2003017.

Chambel M.R., Climent J., Alía R., Valladares F., 2005. Phenotypic plasticity: a useful framework for understanding adaptation in forest species. Invest Agrar: Sist Recur For 14(3), 334-344.

Chuine I., Aitken S.N., Ying C.C., 2001. Temperature thresholds of shoot elongation in provenance of Pinus contorta. Can J For Res 31, 1444-1455. doi: 10.1139/cjfr-31-8-1444.

Chuine I., Rehfeldt G.E., Aitken S.N., 2006. Height growth determinants and adaptation to temperature in pines: a case study of Pinus contorta and Pinus monticola. Can J For Res 36, 1059-1066. doi: 10.1139/X06-005.

Climent J., Chambel M.R., López R., Mutke S., Alía R., Gil L., 2006. Population divergence for heteroblasty in the Canary island pine (Pinus canariensis, Pinaceae) Am J Bot 93(6), 840-848. PMid:21642146

Costa-Silva J., Dutkowski G.W., Gilmour A.R., 2001. Analysis of early tree height in forest genetic trials is enhanced by including a spatially correlated residual. Can J For Res 31, 1887-1893. doi: 10.1139/cjfr-31-11-1887.

Court-Picon M., Gadbin-Henry C., Guibal F., Roux M., 2004. Dendrometry and morphometry of Pinus pinea L. in Lower Provence (France): adaptability and variability of provenances. For Ecol Manag 194, 319-333.

Dutkowski G.W., Costa-Silva J., Gilmour A.R., Lopez G.A., 2002. Spatial analysis methods for forest genetic trials. Can J For Res 32, 2201-2214. doi: 10.1139/x02-111.

Dutkowski G.W., Costa-Silva J., Gilmour A.R., Lopez G.A., Wellendorf H., Aguiar A., 2006. Spatial analysis enhances modelling of a wide variety of traits in forest genetic trials. Can J For Res 36, 1851-1870. doi: 10.1139/X06-059.

Fallour D., Fady B., Lefevre F., 1997. Study of isozyme variation in Pinus pinea L.: evidence for low polymorphism. Silvae Geneticae 46, 201-207.

Fox J.C., Bi H., Ades P.K., 2008. Modelling spatial dependence in an irregular natural forest. Silva Fenn 42, 35-48.

Geng Y.P., Pan X.Y., Xu C.Y., Zhang W.J., Li B., Chen J.K., 2006. Phenotypic plasticity of invasive Alternanthera philoxeroides in relation to different water availability, compared to its native congener. Acta Oecol 30, 380-385.

Gezan S.A., Huber D.A., White T.L., 2006. Post hoc blocking to improve heritability and precision of best linear unbiased genetic predictions. Can J For Res 36(9), 2141-2147. doi: 10.1139/X06-112.

Gordo J., Mutke S., Gil L., 2007. Ausencia de diferenciación ecotípica entre rodales selectos de pino piñonero en la cuenca del Duero. Invest Agrar: Sist Recur For 16(3), 253-261.

Grotkopp E., Rejmánek M., Rost T.L., 2002. Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Am Nat 159, 396-419. PMid:18707424

Hamann A., Namkoong G., Koshy M.P., 2002. Improving precision of breeding values by removing spatially autocorrelated variation in forestry field experiments. Silvae Genetica 51(5-6), 210-215.

Klaus W., 1989. Mediterranean pines and their history. Plant Syst Evolu 162, 133-163.

Kleunen M. Van, Fischer M., 2005. Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166, 49-60. doi: 10.1111/j.1469-8137.2004.01296.x.

Kvaalen H., Johnsen Ø., 2008. Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytol 177(1), 49-59. doi: 10.1111/j.1469-8137.2007.02222.x.

Li W., Wang B., Wang J., 2006. Lack of genetic variation of an invasive clonal plant Eichhornia crassipes in China revealed by RAPD and ISSR markers. Aqu Bot 84, 176-180.

Loo-Dinkins J., 1992. Field test design. In: Handbook of quantitative forest genetics (Fins L., Friedman S.T., Brotschol J.V., eds). Forestry Sciences 39, Kluwer Academics Publishers, Dordrecht. pp. 96-139.

López R., Zehavi A., Climent J., Gil L., 2007. Contrasting ecotypic differentiation for growth and survival in Pinus canariensis. Austral J Bot 55(7), 759-769.

Martin S., Prada A., 1995. Ensayo de procedencias de pino piñonero (Pinus pinea L.) en España. In: El pino piñonero como árbol productor de frutos secos en los países meditarráneos. I Reunión de la Red de Frutos Secos de la FAO sobre el Pino Piñonero, INIA, Madrid. pp. 117-121.

Muñoz-Reinoso J.C., 2004. Diversity of maritime juniper woodlands. For Ecol Manage 192(2/3), 267-276.

Mutke S., Gordo J., Climent J., Gil L., 2003. Shoot growth and phenology modelling of grafted stone pine (Pinus pinea L.) in inner Spain. Ann For Sc 60, 527-537. doi: 10.1051/forest:2003046.

Mutke S., Iglesias S., Gil L., 2007. Selección de clones de pino piñonero sobresalientes en la producción de piña.Invest Agrar: Sist Recur For 16(1), 39-51.

Noel F., Machon N., Porcher E., 2007. No genetic diversity at molecular markers and strong phenotypic plasticity in populations of Ranunculus nodiflorus, an endangered plant species in France. Annals of Botany 99, 1203-1212. PMid:17468109 PMCid:3244344

Peperkorn R., Werner C., Beyschlag W., 2005. Phenotypic plasticity of an invasive acacia versus two native Mediterranean species. Functional Plant Biology 32, 933-944.

Piepho H.P., Richter C., Williams E., 2008. Nearest neighbour adjustment and linear variance models in plant breeding trials. Biom J 50, 164-189. PMid:18383446

Prada M.A., Gordo J., De Miguel J., Mutke S., Catalán G., Iglesias S., Gil L., 1997. Las regiones de procedencia de Pinus pinea L. en España. Organismo Autónomo de Parques Naturales, Madrid.

Rejmánek M., Richardson D.M., 2003. Invasiveness of conifers: extent and possible mechanisms. Acta Horticulturae 615, 375-380.

Rodrigo A., Quintana V., Retana J., 2007. Fire reduces Pinus pinea distribution in the northeastern Iberian Peninsula. Ecoscience 14(1), 23-30.[23:FRPPDI]2.0.CO;2

Schweinfurth G., 1884. Further discoveries in the flora of ancient Egypt. Nature 29, 312-315.

Søgaard G., Johnsen Ø., Nilsen J., Juntilla O., 2008. Climatic control of bud burst in young seedlings of nine provenances of Norway spruce. Tree Phys 28, 311-320. PMid:18055441

St. John L., 2001. Hybrid Poplar - An alternative crop for the intermountain west. USDA-NRCS Plant Materials Technical Notes 37. Aberdeen Plant Materials Center, Aberdeen, ID. PMCid:2094836

Sultan S.E., 2000. Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5, 537-542. doi: 10.1016/S1360-1385(00)01797-0.

Tomback D.F., Linhart Y.B., 1990. The evolution of bird-dispersed pines. Evol Ecol 4, 185-219.

Valladares F., Balaguer L., Martínez-Ferri E., Pérez-Corona E., Esteban Manrique E., 2002. Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phyt 156, 457-467.

Vendramin G.G., Fady B., González-Martínez S.C., Hu F.S., Scotti I., Sebastiani F., Soto A., Petit R.J., 2008. Genetically depauperate but widespread: the case of an emblematic mediterranean pine. Evolution 62(3), 680-688. PMid:17983461

Zas R., 2006. Iterative kriging for removing spatial autocorrelation in analysis of forest genetic trials. Tree Genet Genomes 2(4), 177-185.

Zas R., 2008. The impact of spatial heterogeneity on selection: a case study on Pinus pinaster breeding seedling orchards. Can J For Res 38, 114-124. doi: 10.1139/X07-099.

Zhang L., Gove J.H., 2005. Spatial Assessment of Model Errors from Four Regression Techniques. Forest Science 51, 334-346.

DOI: 10.5424/fs/2010193-9097