# Adaptive effects of geographic origin on tree ring width and radial growth -climate relationships in Pinus nigra Arnold, the European black pine

Guia Giovannelli, Clara Tallieu, Hendrik Davi, Frédéric Guibal, Caroline Scotti-Saintagne, Bruno Fady

► To cite this version:

Guia Giovannelli, Clara Tallieu, Hendrik Davi, Frédéric Guibal, Caroline Scotti-Saintagne, et al.  
Adaptive effects of geographic origin on tree ring width and radial growth -climate relationships in  
Pinus nigra Arnold, the European black pine. 2026. hal-05528456

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For the purpose of Open Access, a CC-BY 4.0 public copyright license has been applied by
the authors to the present document (https://creativecommons.org/licenses/by/4.0/).

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Title: Adaptive effects of geographic origin on tree ring width and
radial growth - climate relationships in *Pinus nigra* Arnold, the
European black pine.

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Authors : Guia Giovannelli¹,², Clara Tallieu¹,³, Hendrik Davi¹, Frédéric Guibal²,
Caroline Scotti-Saintagne¹, Bruno Fady¹

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Addresses:

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¹: INRAE, UR629, Ecologie des Forêts Méditerranéennes (URFM), Domaine Saint Paul,
84914 Avignon, France.

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²: IMBE, Aix Marseille Univ, Avignon Univ, CNRS, IRD, Technopôle de l'environnement
Arbois Méditerranée, Avenue Louis Philibert, 13545 Aix en Provence, France.

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³: Région Grand Est, Direction de l'Eau, de la Biodiversité et du Climat, Service Biodiversité,
1 place Adrien Zeller, BP 91006, 67070 Strasbourg Cedex.

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Abstract

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Radial growth is an adaptive trait that is expected to vary among forest tree populations when habitat conditions change. *Pinus nigra* J.F. Arnold (1785), the European black pine, is a forest tree species widely but patchily distributed throughout southern Europe, from isolated locations in north Africa to the Black Sea and Western Asia. While it has been widely used as plantation species since the mid-19th century because of its strong growth on rather poor soils, the effect of genetic lineages and geographic origins on mean ring widths has not yet need assessed. In
this study, we analyze the radial growth performance of sixteen different geographic origins (provenances) of *P. nigra* growing in four bioclimatically contrasted common gardens in France.

Using a tree-ring to climate relationship approach and a 40-year long chronology, we first estimated how variable the effect of monthly climate was on radial growth, depending on phylogenetic or geographic origin, and plantation habitat. We then used the tree ring data to estimate genetic and plasticity effects and to test for the existence of genotype by environment interactions. Lastly, we ranked the growth performance of the different subspecies and provenances measured in each common garden, having in mind a typology for forest management.

Results showed few climate effect differences among provenances and subspecies, with late spring minimum temperatures affecting radial growth negatively and early summer precipitations positively, overall. Winter maximum temperatures affected radial growth differently depending on the site, with a negative correlation at the warmest sites and a positive correlation at the coldest one. The provenance effect was stronger than the subspecies effect and radial growth phenotypic plasticity was high across the four sites (up to 50% increase in mean tree ring width from low to high fertility sites). While some provenances of *P.n.* subsp. *pallasiana*, *P.n.* subsp. *laricio* and *P.n.* subsp. *nigra* performed well in all sites, others attributed to the same subspecies displayed significant genotype by environment interactions. Provenances of the subspecies *P.n.* subsp. *salzmannii* often displayed the smallest mean ring widths except in the least fertile test site.

Provenance variability within subspecies and not just subspecies variability should be considered in plantation forestry, both for restoration and timber production.

**Keywords:** European black pine, radial growth, provenance test, climate change, dendroecology.
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**Introduction**

Radial (or secondary) growth is an adaptive, fitness-related trait in forest trees that is expected to vary among populations if habitat conditions are variable (Eilmann et al. 2014, Gárate-Escamilla et al. 2019, Latreille et al. 2017). Radial growth is frequently measured using tree ring width in relation to age as it correlates well with biomass production, a trait of high interest in forestry (Campbell et al. 2004, Graumlich et al. 1989). It is also measured to decipher past climate variations and, conversely, analyze the effects of climate on growth patterns across time (Fritts 1971, Rathgeber et al. 2000). Understanding how radial growth of not just species but also their different populations and geographic origins, reacts to climate is particularly important in a context of rapidly changing climate and adaptive management techniques that increasingly advocate the use of assisted migration, the translocation of potentially pre-adapted material to future, warmer climates (Chakraborty et al. 2024, Gray et al. 2011, Housset et al. 2018, Klisz et al. 2019, Palik et al. 2022, Wang et al. 2022).

Common garden tests are a widely employed experimental tool for the investigation of genetic variability, genotype by environment interaction and phenotypic plasticity of fitness-related traits (Schwinning et al. 2022, Taïbi et al. 2014, Vitasse et al. 2010). Provenance tests, a particular type of common garden, are composed of plant material (often seed lots) of known geographic origin collected from (reputedly) unrelated seed trees.

Provenances that have evolved local adaptations will express diverging phenotypes in a common garden. Replicated in common gardens under different environmental conditions, provenance diverging performances will indicate phenotypic plasticity and genotype x environment interaction (de Villemereuil et al. 2016, Fady & Rihm 2022, Langlet 1971). Provenance tests can thus provide key genetic and phenotypic information with minimized confounding environmental effects, about the performance of populations from diverse geographical and climatic origins (Varelides et al. 2001), making it possible to improve forest genetic resource conservation and deploy adapted reproductive materials for reforestation programs (Koskela et al. 2014, Vinceti et al. 2020, Woolridge et al. 2023).

*Pinus nigra* J.F. Arnold (1785), the European black pine, belongs to the family *Pinaceae*, genus *Pinus* and subgenus *Pinus* (Mirov 1967, Price et al. 1998). Its current distribution extends from isolated locations in North Africa eastwards to larger populations across southern and central Europe and to Türkiye and Crimea, covering a wide range of soil types, topographic
conditions and climates (Isajev et al. 2004, Zaghi 2008). Its currently large but highly fragmented geographic distribution contrasts with its relatively limited genetic differentiation and high levels of admixture which result from incomplete lineage sorting during the Pleistocene glacial cycles and recent divergence during the Holocene (Bogunic et al. 2007, Scotti-Saintagne et al. 2019). Plantations using material of unknown origin during the 19th and 20th centuries may have locally further admixed populations (Scotti-Saintagne et al. 2023). As a result, morphological, anatomical and physiological traits are highly variable within geographic origins (Isajev et al. 2004, Naydenov et al. 2006) and complicate taxonomy, with nomenclatures recognizing two to seven subspecies-level taxa (Enescu et al. 2016, Fukarek 1958). International taxonomic authorities such as The Catalogue of Life (http://www.catalogueoflife.org/), Plant the World Online (https://powo.science.kew.org/) or Euro+Med PlantBase (https://europlusmed.org/), based on the morphological and biogeographic work of Gaussen et al. (1964), recognize five subspecies, from west to east: *Pinus nigra* subsp. salzmannii (Dunal) Franco in North Africa, Spain and continental France, *Pinus nigra* subsp. laricio (Poir.) Maire in Corsica (France), Calabria and Sicily (Italy), *Pinus nigra* subsp. dalmatica (Vis.) Franco on the coast of Croatia, *Pinus nigra* subsp. nigra in northern Italy, Austria and most of Central Europe and the western Balkans, and *Pinus nigra* subsp. pallasiana (Lamb.) Holmboe in parts of Greece and the eastern Balkans, Cyprus, Türkiye and Crimea. The most recent phylogenetic study of the species (Scotti-Saintagne et al. 2019) identified six lineages, splitting *P.n.* subsp. *pallasiana* into two distinct genetic groups, one homogeneous in Cyprus and one relatively admixed encompassing all other eastern Mediterranean and Black Sea populations, confirming results obtained from common gardens (Wheeler et al. 1976) and isozyme analyses (Nikolić & Tucić 1983).

Several dendroclimatic studies have shown that black pine is sensitive to high summer temperatures and to water deficit during spring and summer (Amodei et al. 2013, Lebourgeois 2000, Martín-Benito et al. 2008). This sensitivity is critical in areas where drought is frequent, such as the Mediterranean region (Génova & Fernández 1999, Lebourgeois 2000, Linares & Tíscar 2011, Martin-Benito et al. 2010, Richter et al. 1991), where an increase in mean temperature and a decrease in precipitation is likely in the foreseeable future (Sumner et al. 2003, Giorgi & Lionello 2008, MedECC 2020). Camarero et al. (2013) showed that, in relict rear-edge *P. nigra* populations in southern Spain and Morocco, growth responses to drought changed along an aridity gradient, and that dry conditions before tree-ring formation constituted the major constrain for growth. Previous studies have also highlighted that *P. nigra* growth in
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Iberian forests was enhanced by wet and cold conditions during the previous autumn and by
warm late winters (Andreu et al. 2007, Martín-Benito et al. 2010). Finally, soil texture and its
relative ability to store water were identified as major drivers for radial growth (Génova &
Martinez-Morillas 2002, Camarero et al. 2013), including at very short spatial scales (Amodei
et al. 2013).

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Yet, little data and few analyses exist about the genetic diversity of the correlation between radial growth and climate in trees. When such tree ring studies exist, they demonstrate variable levels of intra-specific variability (Oleksyn et al. 1998, Savva et al. 2008, Sang et al. 2019) and provide predictions for the risks associated with seed transfer used a climate change adapted management strategy (e.g. Savva et al. 2007). In black pine, and typically for forest trees (Park & Rogers 2023), most multi-site common gardens were established with the aim of providing information on the best seed sources for plantation forestry and as a basis for breeding, focusing on traits such as mortality, height and diameter growth, and resistance to insects and pathogens.
Results showed that variation in growth traits was high among subspecies and provenances.
They also tended to demonstrate a stronger hardiness in *Pinus nigra* subsp. *nigra*, and fast growth, slender branches and higher volume in *P.n.* subsp. *laricio* in high fertility, milder climate sites (Kreyling et al. 2012, Seho et al. 2010, Wheeler et al. 1976, Wilcox & Miller 1975).
Most of these experiments poorly sampled the easternmost and westernmost *Pinus nigra* lineages (but see Varelides et al. 2001) and led to breeding programs focused on Corsican black pine (Lee & Connolly 2004, Portefaix et al. 1987, Portefaix 1989), while Austrian black pine was mostly used in erosion control, restoration projects (Vallauri et al. 2002).

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The objective of our study is to describe and understand how variable the effect of monthly climate is on the radial growth of the European black pine, depending on phylogenetic or geographic origin, and plantation habitat. Using annual tree ring data and genetic material replicated in four common gardens, we assess provenance and subspecies effect on tree ring width and test for the presence of phenotypic plasticity and genotype x environment interaction.
Lastly, having in mind a typology for forest management, we discuss if forest reproductive material recommendations for planting should be made at provenance rather than subspecies level, as usually done.

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149 Radial growth data were collected from four sites located in different habitats covering the 150 main bioclimatic zones of France (Table 1, Figure 1): Cestas in southwestern France (oceanic 151 climate), Levens in southeastern France (Mediterranean mountain climate), Pomet (two 152 adjacent common gardens each with different provenances) in southeastern France (peri- 153 Mediterranean climate with a slight water deficit during the summer) and Verdun (two adjacent 154 common gardens each with different provenances) in northeastern France (continental climate).

155 **Figure 1:** Ombrothermic diagrams of the four Pinus nigra experimental sites. The 156 temperature scale is twice that of the precipitation scale. Precipitations are featured as blue 157 bars, temperatures as red curves. Months are numbered from January onward.

<figure><img src="image_2.png" /></figure>

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The common gardens were planted in each site between 1968 and 1974 with the initial 159
purpose of comparing the performance of provenances and subspecies for breeding and forest 160
reproductive material selection in environmental conditions where black pine plantation forests 161
were a target of management, both for wood production and erosion control. Cestas and Pomet 162
are part of a series (exact same provenances planted during the same campaign) while Levens 163
and Verdun are part of another one. It is unclear whether the provenances that are common 164
between the two series come from a single seed lot or from two different seed lots collected 165
from the same place but at different times. 166
<table><caption>Table 1: Common garden sites selected for the study and their main characteristics (* trial design: BICA: incomplete blocks with random composition; BC: complete blocks). Common garden characteristics are described in detail in Fady et al. (2024).</caption><thead><tr><th>Site name</th><th>Cestas</th><th>Levens</th><th>Pomet</th><th>Verdun</th></tr></thead><tbody><tr><td>Common garden code in Fady et al (2024)</td><td>01-4200-09-02</td><td>01-4200-02-01</td><td>01-4200-09-03 (latt / mono)</td><td>01-4200-02-03 / 01-4200-06-03</td></tr><tr><td>Bioclimate</td><td>Oceanic</td><td>Mountain</td><td>Supra-Mediterranean</td><td>Continental</td></tr><tr><td>Latitude (degree decimal)</td><td>44.7388</td><td>43.8775</td><td>44.2926</td><td>49.2111</td></tr><tr><td>Longitude (degree decimal)</td><td>-0.7623</td><td>6.2939</td><td>5.7952</td><td>5.4496</td></tr><tr><td>Elevation (m)</td><td>58</td><td>1332</td><td>838</td><td>335</td></tr><tr><td>Aspect</td><td>Flat</td><td>North-West</td><td>South-West</td><td>Flat</td></tr><tr><td>Substrate</td><td>Sedimentary sil-ica</td><td>Sedimentary limestone</td><td>Sedimentary limestone</td><td>Sedimentary limestone</td></tr><tr><td>Site status</td><td>Private (INRAE)</td><td>State forest</td><td>State forest</td><td>State forest</td></tr><tr><td>Plantation date (year-month-day)</td><td>1974-03-06</td><td>1968-Spring</td><td>1973-Fall</td><td>1968-03-08 / 1971-05-28</td></tr><tr><td>Trial design*</td><td>CB</td><td>BICA</td><td>BICA / CB</td><td>BICA</td></tr><tr><td>Seedlings age at plantation time</td><td>2+0</td><td>1+2</td><td>1+1</td><td>1+2</td></tr><tr><td>Mean annual precipitation (mm)</td><td>980</td><td>840</td><td>763</td><td>882</td></tr><tr><td>Mean annual temperature (°C)</td><td>12.3</td><td>7.4</td><td>10.2</td><td>9</td></tr><tr><td>Mean monthly minimum temperature (°C)</td><td>5.7</td><td>-1</td><td>1.1</td><td>1.3</td></tr><tr><td>Mean monthly maximum temperature (°C)</td><td>19.6</td><td>16.8</td><td>19.9</td><td>17.2</td></tr><tr><td>Initial spacing (m)</td><td>4x1.1</td><td>2x2</td><td>2x2</td><td>2x2</td></tr><tr><td>Total area (ha)</td><td>2.21</td><td>4.83</td><td>0.96 / 0.53</td><td>3.2 / 3.46</td></tr><tr><td>Number of provenances</td><td>105</td><td>31</td><td>25 / 19</td><td>31 / 25</td></tr><tr><td>Number of blocks</td><td>7</td><td>30</td><td>30 / 70</td><td>36 / 30</td></tr><tr><td>Number of plots per block</td><td>105</td><td>6</td><td>5 / 19</td><td>6 / 5</td></tr><tr><td>Number of trees per plot</td><td>6</td><td>56</td><td>16 / 1</td><td>25 / 36</td></tr><tr><td>Number of trees per test</td><td>4716</td><td>10109</td><td>2400 / 1330</td><td>5400 / 5410</td></tr><tr><td>Mortality in % in 2014</td><td>75</td><td>60</td><td>6 / 6</td><td>28 / 34</td></tr></tbody></table>

Sixteen provenances from a large part of the European geographic range of *Pinus nigra* were selected for this study (Table 2). Most of the provenances were present in at least three of the four sites and seven were present in all sites. The sixteen provenances belonged to four black pine subspecies: *P.n.* subsp. *salzmannii*, *P.n.* subsp. *laricio*, *P.n.* subsp. *nigra* and *P.n.* subsp. *pallasiana* (Table 2). Together, they sample all genetic lineages described in *Pinus nigra*, either as pure or admixed provenances, the admixture likely the result of ancient, natural contacts
178 between genetic groups, although plantations using mixed origins cannot entirely be excluded
179 (Scotti-Saintagne 2019).

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<table><caption>Table 2: Pinus nigra provenances selected for the study and their main geographic characteristics. Genetic group is according to Figure 3 of Scotti-Saintagne et al. (2019) where six different genetic groups are identified range-wide. Sample size indicates the number of trees for which there are usable tree ring data in the dataset in Fady et al. (2024).</caption><thead><tr><th rowspan="2">Provenance name</th><th rowspan="2">Provenance Code</th><th rowspan="2">Subspecies</th><th rowspan="2">Country</th><th rowspan="2">Genetic group</th><th colspan="3">Geographic coordinates</th><th colspan="4">Sample size in each common garden</th></tr><tr><th>Latitude</th><th>Longitude</th><th>Altitude (m)</th><th>Cestas</th><th>Levens</th><th>Pomet</th><th>Verdun</th></tr></thead><tbody><tr><td>Aspromonte</td><td>ASPR</td><td>P.n. laricio</td><td>Italy</td><td>2</td><td>38°05'N</td><td>16°00'E</td><td>1300</td><td>11</td><td>13</td><td>17</td><td>18</td></tr><tr><td>Cosenza</td><td>COSE</td><td>P.n. laricio</td><td>Italy</td><td>2+3</td><td>39°15'N</td><td>16°17'E</td><td>1300</td><td>11</td><td>15</td><td>22</td><td>16</td></tr><tr><td>Valdoniello</td><td>VALD</td><td>P.n. laricio</td><td>France</td><td>2</td><td>41°51'N</td><td>9°06'E</td><td>1100</td><td>8</td><td>16</td><td>17</td><td>19</td></tr><tr><td>Doblhoff</td><td>DOBL</td><td>P.n. nigra</td><td>Austria</td><td>3</td><td>48°00'N</td><td>16°13'E</td><td>280</td><td>5</td><td>na</td><td>20</td><td>na</td></tr><tr><td>Perithorion</td><td>PERT</td><td>P.n. nigra</td><td>Greece</td><td>3</td><td>38°05'N</td><td>22°15'E</td><td>1300</td><td>5</td><td>na</td><td>21</td><td>na</td></tr><tr><td>Studenica</td><td>STUD</td><td>P.n. nigra</td><td>Serbia</td><td>3+4</td><td>43°30'N</td><td>20°33'E</td><td>930</td><td>9</td><td>na</td><td>18</td><td>16</td></tr><tr><td>Thasos</td><td>THAS</td><td>P.n. nigra</td><td>Greece</td><td>4+5</td><td>40°40'N</td><td>24°40'E</td><td>850</td><td>12</td><td>na</td><td>22</td><td>18</td></tr><tr><td>Tzarvaritza / Kustendil</td><td>TZKU</td><td>P.n. nigra</td><td>Bulgaria</td><td>3</td><td>42°01'N</td><td>22°50'E</td><td>1050</td><td>10</td><td>15</td><td>16</td><td>37</td></tr><tr><td>Aluchtin</td><td>CRIM</td><td>P.n. pallasiana</td><td>Crimea</td><td>5</td><td>44°33'N</td><td>34°17'E</td><td>500</td><td>6</td><td>16</td><td>20</td><td>29</td></tr><tr><td>Ayanick</td><td>AYAN</td><td>P.n. pallasiana</td><td>Türkiye</td><td>5</td><td>41°43'N</td><td>34°31'E</td><td>1400</td><td>6</td><td>16</td><td>17</td><td>19</td></tr><tr><td>Popova-Livada</td><td>POLV</td><td>P.n. pallasiana</td><td>North Macedonia</td><td>3+4</td><td>41°10'N</td><td>21°55'E</td><td>1450</td><td>8</td><td>na</td><td>17</td><td>17</td></tr><tr><td>Yilanli / Mugla</td><td>YIMU</td><td>P.n. pallasiana</td><td>Türkiye</td><td>4+5+6</td><td>37°20'N</td><td>28°24'E</td><td>975</td><td>10</td><td>na</td><td>19</td><td>17</td></tr><tr><td>Cazorla</td><td>CAZO</td><td>P.n. salzmannii</td><td>Spain</td><td>1</td><td>37°50'N</td><td>3°00W</td><td>1500</td><td>na</td><td>15</td><td>na</td><td>15</td></tr><tr><td>Fresneda</td><td>FRES</td><td>P.n. salzmannii</td><td>Spain</td><td>1</td><td>40°23'N</td><td>2°08'W</td><td>1025</td><td>9</td><td>na</td><td>21</td><td>19</td></tr><tr><td>Priego</td><td>PRIE</td><td>P.n. salzmannii</td><td>Spain</td><td>1</td><td>40°27'N</td><td>2°18'W</td><td>850</td><td>9</td><td>na</td><td>21</td><td>na</td></tr><tr><td>St.Guilhem / Gagnières</td><td>GAS-GUL</td><td>P.n. salzmannii</td><td>France</td><td>2</td><td>44°07'N</td><td>4°17'E</td><td>350</td><td>16</td><td>31</td><td>22</td><td>28</td></tr></tbody></table>

Provenance and site metadata are described and available open access in Fady et al. (2024).

Please note that the code names GASGUL, TZKU and YIMU are not found in Fady et al. (2024). They indicate that provenances originally named differently (St.Guilhem / Gagnières, Tzarvaritza / Kustendil, and Yilanli / Mugla, respectively) were grouped into a single provenance as they have the same geographic origin.

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Sampling of tree rings

Annual tree ring widths were measured on wood cores collected in 2014 on a subset of 16 individuals per provenance in each common garden on average (Table 2), using a Swedish
increment borer mounted on a combustion engine (Grissino-Mayer, 2003). We sampled two radii per individual at breast height. As radial growth is sensitive to competition and social status (Lebourgeois et al. 2014, Martín-Benito et al. 2008), we selected healthy, dominant and cylindrical trees without forking defects, surrounded by an equal number of four codominant neighbors. Mortality (excluding thinned trees) in 2014 was very high at Cestas (Table 1) because of two successive wind storms (1999 and 2009), leading to the presence of fewer trees there complying to these requirements than in the other three common gardens. In Levens, mortality was high but it affected only some of the blocks (water logging).

The collected cores were dried at room temperature for one month and then sanded. Ring width was measured with a precision of 1/100th mm using LinTabTM, a robust and precise station for the measurement of ring width series for increment cores in association with a Leica stereo microscope and the TSAP-WIN software (Frank Rinn®). Individual annual ring widths (rw) were calculated as the mean of the two radii collected on each tree. Tree ring width data and their associated metadata are available open access in Fady et al. (2024).

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209 Climate data

Climatic data were collected from SAFRAN® (Système d'Analyse Fournissant des Renseignements Adaptés à la Nivologie), a reanalysis dataset initially designed to provide atmospheric forcing data in mountainous areas for avalanche hazard forecasting (Durand et al. 1993) and successively extended to feed macroscale soil-vegetation-atmosphere transfer models over the whole France (Le Moigne 2002). SAFRAN provides hourly climatic data with a resolution of 8 km using the Lambert-II projection (Pagé 2008). Climatic data were collected, for each of the four sites, for the period extending from 1959 to 2013. The period is characterized by some exceptional years, such as 1976 (summer drought except in southern France) and 2003 (summer heat wave).

To estimate relationships between ring width and climate and account for black pine's known sensitivity to high summer temperatures and water deficit during spring and summer (Amodei et al. 2013, Lebourgeois 2000, Martín-Benito et al. 2008), we selected monthly variables potentially able to limit the European black pine radial growth: mean minimal and maximal temperature and the monthly precipitations.
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Climate data and their associated metadata are available open access in Fady et al. (2024).

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<caption>Figure 2: Growth chronology curves spanning four decades made of individual ring width raw data aggregated as means at four different test sites for four Pinus nigra subspecies.</caption>

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<figure><img src="image_3.png" /></figure>

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## Data analysis

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Data analysis was carried out considering adjacent common gardens within the same site (i.e., Pomet and Verdun) as a single analytical unit. We used the datasets containing all provenances, thus replicated two to four times across sites, to analyze overall climate-growth trends and genetic diversity at subspecies and provenance levels. To assess phenotypic plasticity and genotype x environment interactions, we used the dataset restricted to the seven provenances present in all sites (Table 2).

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Effect of climate on tree ring width

To identify the relationships between climatic variables and radial growth, individual ring width series were standardized using the “detrend series” function of the R package “dplR” (Bunn et al. 2016). The detrending estimates and removes the low and intermediate frequency variability due, for example, to biological (ontogenic stage) effects (Figure 2). This is done by dividing each series by the growth trend to produce dimensionless ring width indices (rwi) with constant mean and standard deviation over time. In this study, ring width series were standardized with the autoregressive method which removes all but the high frequency variation in the series, a procedure well adapted to short chronologies such as ours. The detrended ring width series were then used to build mean individual, provenance and subspecies chronologies using the “chron” function of the R package “dplR” (Bunn et al. 2016). Pearson’s correlation coefficients were then calculated between each mean chronology and their corresponding monthly climatic variables over a twelve-month period, from October of the previous year to September of the current year, using the “dcc” function of the R package “bootRes” (Zang & Biondi 2012) which adjusts results for multiple testing.

Effect of subspecies and provenance on tree ring width

We estimated provenance and subspecies effects using a simple analysis of variance (ANOVA) model and the “lmer” function in R (R Core Team 2015), as follows:

$$Y = \mu + P + B + \varepsilon$$

where Y is the individual tree ring width (rw), μ is the general mean, P is the provenance (or subspecies) random effect, B is the random block effect in each site and ε is the error term. We did not nest provenances within subspecies as many provenances are often admixed (Table 2) between at least two genetic clusters corresponding to subspecies (Scotti-Saintagne et al. 2019). Also, as recommendations for forest reproductive materials (FRM) are often done at subspecies levels, we wanted to measure variance components for provenances and subspecies independently to analyze if provenance level FRM recommendations would not be preferable than subspecies level FRM recommendations.

Due to our experimental constraint of using individuals surrounded by four neighbors, provenance sample replication within block was uneven in the different sites. However, provenances were always replicated at least once in at least two different blocks. Block design
268

was treated as incomplete in all sites. To avoid biases linked to normal distribution assumptions,
we compared provenance means using a Kruskal-Wallis test and the post-hoc Wilcoxon Mann
Whitney procedure.

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270

271

To test for the existence of phenotypic plasticity, we compared provenance variance across
sites, with the assumption that equal provenance effects would indicate an absence of
phenotypic plasticity. We tested for genotype x environment (GxE) interactions using response
curves, where tree ring width mean values per provenance were ranked within site, with the
assumption that rank changes across sites would indicate GxE interaction.

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274

275

276

277

## Results

278

### Climate-growth relationships

279

We obtained high quality annual ring width data with a precision to the 0.01 mm spanning
the period 1970 to 2013 from 867 individuals sampled from all common gardens (Table 3).
Mean ring width was 3.02 mm. It varied from 2.51 mm in Pomet to 3.31 in Levens, from 2.76
mm in Salzmann's pine to 3.12 mm in Austrian black pine, and from 2.26 mm in provenance
PERT to 3.24 mm in provenance AYAN.

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<table><caption>Table 3: Ring width mean, minimum and maximum values (mm, 1970 to 2013) obtained for the four subspecies and the sixteen provenances of P. nigra within each test site. The seven provenances found in all test sites are in bold and the significance of the differences of their mean tree ring widths are indicated by different letters (Kruskal-Wallis test, “a” denoting the significantly higher value group).</caption><thead><tr><th></th><th>Sites</th><th>CESTAS</th><th>LEVENS</th><th>POMET</th><th>VERDUN</th><th>Mean</th></tr></thead><tbody><tr><td></td><td>Mean (min / max)</td><td>3.21 (1.25 / 5.16)</td><td>3.31 (2.02 / 4.82)</td><td>2.51 (1.55 / 4.00)</td><td>3.04 (1.58 / 4.84)</td><td>3.02</td></tr><tr><td rowspan="4">Subspecies</td><td><i>P.n. laricio</i></td><td>3.59</td><td>3.26</td><td>2.48</td><td>3.07</td><td>3.1</td></tr><tr><td><i>P.n. nigra</i></td><td>3.31</td><td>3.28</td><td>2.55</td><td>3.33</td><td>3.12</td></tr><tr><td><i>P.n. pallasiana</i></td><td>3.02</td><td>3.49</td><td>2.58</td><td>3.09</td><td>3.05</td></tr><tr><td><i>P.n. salzmannii</i></td><td>2.89</td><td>3.14</td><td>2.34</td><td>2.65</td><td>2.76</td></tr><tr><td rowspan="15">Provenances</td><td>ASPR</td><td>3.48 <i>a</i></td><td>3.18 <i>d</i></td><td>2.38 <i>b</i></td><td>2.94 <i>d</i></td><td>2.99</td></tr><tr><td>COSE</td><td>3.71 <i>a</i></td><td>3.4 <i>b</i></td><td>2.63 <i>a</i></td><td>3.19 <i>abc</i></td><td>3.23</td></tr><tr><td>VALD</td><td>3.59 <i>a</i></td><td>3.19 <i>d</i></td><td>2.36 <i>b</i></td><td>3.09 <i>cd</i></td><td>3.06</td></tr><tr><td>TZKU</td><td>3.29 <i>ab</i></td><td>3.28 <i>c</i></td><td>2.74 <i>a</i></td><td>3.27 <i>a</i></td><td>3.15</td></tr><tr><td>AYAN</td><td>3.6 <i>ab</i></td><td>3.5 <i>a</i></td><td>2.72 <i>a</i></td><td>3.12 <i>bcd</i></td><td>3.24</td></tr><tr><td>CRIM</td><td>3.05 <i>bc</i></td><td>3.81 <i>a</i></td><td>2.45 <i>b</i></td><td>3.24 <i>ab</i></td><td>3.14</td></tr><tr><td>GASGUL</td><td>2.81 <i>c</i></td><td>3.14 <i>d</i></td><td>2.18 <i>c</i></td><td>2.45 <i>e</i></td><td>2.65</td></tr><tr><td>DOBL</td><td>2.86</td><td>na</td><td>2.25</td><td>na</td><td>2.56</td></tr><tr><td>PERT</td><td>2.18</td><td>na</td><td>2.33</td><td>na</td><td>2.26</td></tr><tr><td>STUD</td><td>3.89</td><td>na</td><td>2.57</td><td>3.23</td><td>3.23</td></tr><tr><td>THAS</td><td>3.45</td><td>na</td><td>2.7</td><td>3.54</td><td>3.23</td></tr><tr><td>POLV</td><td>2.76</td><td>na</td><td>2.55</td><td>2.8</td><td>2.70</td></tr><tr><td>YIMU</td><td>2.95</td><td>na</td><td>2.59</td><td>3.13</td><td>2.89</td></tr><tr><td>CAZO</td><td>na</td><td>3.11</td><td>na</td><td>2.82</td><td>2.97</td></tr><tr><td>FRES</td><td>2.83</td><td>na</td><td>2.73</td><td>2.8</td><td>2.79</td></tr><tr><td>PRIE</td><td>3.1</td><td>na</td><td>2.51</td><td>na</td><td>2.81</td></tr></tbody></table>

At species level, aggregated data showed significant negative correlations between growth and late spring maximum temperatures at all sites except Levens, the coldest, highest elevation site where growth-climate correlations were rarely significant(). Growth was negatively correlated to winter maximum temperatures at the warmest sites (Cestas, Pomet) and positively (February) at Verdun, the continental site. Growth was negatively correlated to late spring minimum temperatures at all sites. The warmest site of Cestas showed a positive correlation with September minimum temperatures while the continental site of Verdun showed a positive correlation with February minimum temperatures. Finally, there was a significant positive correlation between June precipitations and radial growth at all sites except Levens, the Mediterranean mountain site.
Figure 3: Positive (green) and negative (orange) correlations between radial growth and maximum (Tmax) and minimum (Tmin) monthly temperatures, and monthly precipitations in four common garden sites. For species and subspecies, data were aggregated using the sixteen-provenance dataset. Months are abbreviated from October onward. Months of the previous year are shown as lower case letters.

<table><thead><tr><th>Tmax</th><th colspan="10">Cestas</th><th colspan="10">Levens</th><th colspan="10">Pomet</th><th colspan="10">Verdun</th></tr><tr><th></th><th>o</th><th>n</th><th>d</th><th>J</th><th>F</th><th>M</th><th>A</th><th>M</th><th>J</th><th>J</th><th>A</th><th>S</th><th>o</th><th>n</th><th>d</th><th>J</th><th>F</th><th>M</th><th>A</th><th>M</th><th>J</th><th>J</th><th>A</th><th>S</th><th>o</th><th>n</th><th>d</th><th>J</th><th>F</th><th>M</th><th>A</th><th>M</th><th>J</th><th>J</th><th>A</th><th>S</th><th>o</th><th>n</th><th>d</th><th>J</th><th>F</th><th>M</th><th>A</th><th>M</th><th>J</th><th>J</th><th>A</th><th>S</th></tr></thead><tbody><tr><td>Pinus nigra</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. laricio overall</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASPR (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>COSE (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>VALD (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. nigra</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>TZKU (nigra)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. pallasiana</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>AYAN (pallasiana)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>CRIM (pallasiana)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. salzmanni</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>SASGUL (salzmannii)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><th>Tmin</th><th colspan="10">Cestas</th><th colspan="10">Levens</th><th colspan="10">Pomet</th><th colspan="10">Verdun</th></tr><tr><td>Pinus nigra</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. laricio</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASPR (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>COSE (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>VALD (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. nigra</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>TZKU (nigra)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. pallasiana</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>AYAN (pallasiana)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>CRIM (pallasiana)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. salzmanni</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>SASGUL (salzmannii)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><th>Prec</th><th colspan="10">Cestas</th><th colspan="10">Levens</th><th colspan="10">Pomet</th><th colspan="10">Verdun</th></tr><tr><td>Pinus nigra</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. laricio</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>ASPR (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>COSE (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>VALD (laricio)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. nigra</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>TZKU (nigra)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. pallasiana</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>AYAN (pallasiana)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>CRIM (pallasiana)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>P.n. salzmanni</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>SASGUL (salzmannii)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

Climate correlations at subspecies level were similar to those aggregated at species level, with some variation depending on site conditions (Figure 3). While negative correlations between growth and late spring maximum temperatures remained significant at all sites except Levens, *P.n.* subsp. nigra showed less sensitivity overall to maximum temperatures at Verdun and Cestas (the wettest sites) than at Pomet (the driest site). At the continental site of Verdun, *P.n.* subsp. nigra showed fewer negative correlations with minimum temperatures while at Pomet and Levens, it was *P.n.* subsp. laricio. As for precipitations, *P.n.* subsp. salzmannii diverged slightly from the general pattern with a negative effect in August and no effect in June at Verdun, and a positive effect of October at Cestas.

Climate correlations at provenance level showed some departures from those aggregated at subspecies level (Figure 3). For example, the *P.n.* subsp. laricio provenances ASPR from Italy and VALD from France (belonging to the same genetic group) were less sensitive to minimum
and maximum temperatures than the admixed *P.n.* subsp. *laricio* provenance COSE from Italy, while in Cestas it was the opposite for minimum temperatures. The three *P.n.* subsp. *laricio* provenances diverged in their reaction to precipitations irrespectively of their genetic group at all sites except Levens where precipitation anomalies did not affect growth. Some divergence between the two *P.n.* subsp. *pallasiana* provenances tested at Levens were found for sensitivity to fall minimum temperatures. The Bulgarian *P.n.* subsp. *nigra* provenance TZKU was less negatively influenced by winter maximum temperatures at Pomet and by summer minimum temperatures at Cestas, than the overall *P.n.* subsp. *nigra* provenance mean. Finally, the French *P.n.* subsp. *salzmannii* provenance GASGUL diverged from the *P.n.* subsp. *salzmannii* overall mean for sensitivity to maximum temperatures during cold months at all sites.

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### Environmental, provenance and subspecies effects on phenotypic trait variation.

Block effects on ring widths were only significant at Pomet (Table 4), and provenance and subspecies means were adjusted to block effects there.

<table><caption>Table 4: Percentages of total phenotypic variance of tree ring width (rw) explained by the subspecies, provenance and respective block effects at the four study sites, using the sixteen-provenance (rw (16)) or the balanced seven-provenance (rw (7)) datasets. Effects statistically significant at the 5% level are indicated by (*).</caption><thead><tr><th></th><th></th><th>rw (16)</th><th>rw (7)</th></tr></thead><tbody><tr><td rowspan="4">Cestas</td><td>Prov</td><td>20.28*</td><td>8.59</td></tr><tr><td>Block/Prov</td><td>2.699</td><td>3.91</td></tr><tr><td>Subsp</td><td>11.33</td><td>11.00*</td></tr><tr><td>Block/Subsp</td><td>1.38</td><td>3.19</td></tr><tr><td rowspan="4">Levens</td><td>Prov</td><td>15.9*</td><td>16.90*</td></tr><tr><td>Blokc/Prov</td><td>9.94</td><td>10.86</td></tr><tr><td>Subsp</td><td>13.13</td><td>11.74</td></tr><tr><td>Block/Subsp</td><td>12.85</td><td>12.88</td></tr><tr><td rowspan="4">Pomet</td><td>Prov</td><td>13.5*</td><td>19.74*</td></tr><tr><td>Block/Prov</td><td>12.1*</td><td>8.97*</td></tr><tr><td>Subsp</td><td>6.25*</td><td>22.03*</td></tr><tr><td>Block/Subsp</td><td>17.33*</td><td>10.18</td></tr><tr><td rowspan="4">Verdun</td><td>Prov</td><td>23.18*</td><td>22.43*</td></tr><tr><td>Block/Prov</td><td>0</td><td>0</td></tr><tr><td>Subsp</td><td>24.65*</td><td>33.65</td></tr><tr><td>Block/Subsp</td><td>3.07</td><td>0</td></tr></tbody></table>

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Subspecies effects were significant in half the sites and explained between 6.25% (Pomet) and 24.65% (Verdun) of ring width variance in the sixteen-provenance dataset. Provenance effects were significant at all sites and explained between 13.5% (Pomet) and 23.18% (Verdun) of ring width variance. Provenance effects were higher than subspecies effects in all sites except Verdun. (Table 4).

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Provenance mean ring width values are shown in Table 3. Subspecies and provenance rankings varied across sites (Figure 4) and provenance differences were often larger than mean subspecies differences in most sites. For example, although *P.n. subsp. laricio* rarely ranked last, provenances attributed to *P.n. subsp. laricio* were often outperformed by at least one provenance attributed to one other subspecies. Within subspecies, rankings were also variable except for COSE and GASGUL which always ranked first and last within the provenances of *P.n. subsp. laricio* and *P.n. subsp. salzmannii*, respectively.
Figure 4: Mean ring width (rw, in mm) over 40 years of growth at all sites for all 16 provenances. Provenances in a blue tone are attributed to subspecies Pinus nigra laricio, those in red tone to P.n. nigra, those in green tone to P.n. pallasiana and those in grey tone to P.n. salzmannii (see Table 2). Vertical bars are standard deviations.

<figure><img src="image_4.png" /></figure>

When restricting the analysis of variance to the seven provenances present at all sites, provenance effects remained significant except at Cestas and were variable among sites, explaining 16.90% to 22.43% of total provenance tree ring width variance when significant (Table 4). Grouping provenances into subspecies, subspecies effects were significant at Cestas and Pomet only and explained 11.00% to 22.03% of total provenance tree ring width variance when significant (Table 4). Overall sites, provenance and subspecies effects varied from non-significant to over 22%, suggesting stronger phenotypic plasticity across sites for provenances than subspecies.

Overall mean rw increased by 32% from the lowest (Pomet) to the highest (Levens and Cestas) fertility sites (Table 3). Considering provenances that were present in all sites, rw increased by 46% for ASPR between Pomet and Cestas, and from 44% for GASGUL to 55% for CRIM between Pomet and Levens, for example. Mean rw variation was mostly irrespective of plantation date, and decreased from the wettest sites to the dryest and hottest site (Pomet). (Figure 4, Figure 5).

The provenances with the highest mean rw over all sites were from different phylogenetic backgrounds: AYAN (*P.n. subsp. pallasiana*, Türkiye), COSE (*P.n. subsp. laricio*, Italy),
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TZKU (*P.n.* subsp. *nigra*, Bulgaria). However, they did not rank first at all sites (Table 3).

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Except for GASGUL (*P.n.* subsp. *salzmannii*, France) which ranked last at all sites., there was

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substantial provenance x site interactions (Figure 5).

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*Figure 5: Norms of reaction for mean ring width (rw) for each of the 7 provenances that were present in all sites. Sites are ordered by increasing fertility, measured by their mean rw.*

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Provenances in a blue tone are attributed to subspecies Pinus nigra laricio, that in red tone to *P.n. nigra*, those in green tone to *P.n. pallasiana* and that in grey tone to *P.n. salzmannii* (see Table 2). Vertical bars are standard deviations.

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<figure><img src="image_5.png" /></figure>

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## Discussion

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### Climate and radial growth

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Radial growth is the result of cambium activity which depends mainly on water and carbon availability, both strongly determined by external climatic conditions (Linares & Tíscar 2010).

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The radial growth of the European black pine was positively correlated with early summer precipitations (June or July) and negatively correlated with spring (March and May) and summer temperatures (June and July) across experimental sites and genotypes, as previously shown by Leal et al. (2008) and Lebourgeois (2000). Other studies have also identified a

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significant positive influence of spring temperatures and early summer precipitations on ring width of black pine in Mediterranean sites (Izmir et al. 2024, Jevšenak & Saražin 2023, Martin-Benito et al. 2010). In Tunisia, at the dry end of the ecological spectrum of Pinus nigra, April precipitations had a significant positive effect on radial growth (Fkiri et al. 2018). These results highlight the fundamental and beneficial role of precipitations during early wood formation when temperatures are starting to reach their maximum, and the negative effects of summer heat and drought in the European black pine (Andreu et al. 2007, Camarero et al. 2013, Lebourgeois 2000).

Site differences for climate effects on radial growth were weak. Perhaps the most striking differences were the opposite positive correlations with winter temperatures at Verdun, the continental site, and negative correlations in other sites, particularly Cestas, the wettest oceanic climate site. This may suggest that under a continental climate, warmer than average winters will increase growth in *P. nigra* as observed in previous studies (Amodei et al. 2013, Andreu et al. 2007). Conversely, too warm winters in mild and wet sites such as Cestas will limit growth, perhaps because of delayed xylem formation or premature dormancy breaking which can expose cambial cell divisions to late spring frost (Begum et al. 2013, Ladwig et al. 2019).

As noted by Fkiri et al. (2018), there were few differences among subspecies and provenances in their sensitivity to monthly precipitations and temperatures. Within species, a notable difference was the positive correlation between growth and October precipitations at Cestas and a negative correlation between growth and August precipitations at Verdun in *P.n*. subsp. *salzmannii*. This could indicate that in wet sites, an excess of precipitations during the Fall season is beneficial to growth of *P.n*. subsp. *salzmannii* while late summer precipitations are not. In the dry calcareous site of Pomet, two *P.n*. subsp. *pallasiana* provenances benefited from late spring precipitations potentially indicating an increased drought resistance in comparison to other black pine subspecies.

## Genetic diversity, differentiation and plasticity

Provenance differences accounted for up to 24% of observed mean ring width variance depending on site. To our knowledge, there are few studies that use common gardens to analyze provenance effect on tree ring width (possibly because old-enough common gardens are rare). In these studies, provenance effects are generally lower than ours, with site effect being the most important factor (George et al. 2019, Matisons et al. 2019, Savva et al. 2007, Unterholzner
et al. 2024). Provenance effect on ring width variance were generally higher than subspecies effects (except in the continental site of Verdun). Among the four sites, Pomet had the lowest provenance effect on ring width variance as well as the weakest performance, indicating that provenance variation decreases when ecological constraints increase (and thus, that choice of material for radial growth might be of lowest concern where black pine reaches its ecological lower limits).

Although our design does not make it possible to measure additive genetic variance and thus formally compare phenotypic trait differentiation due to selection from that due to genetic drift (Leinonen et al. 2013), the differentiation measured in Scotti-Saintagne et al. (2019) on a slightly geographically wider set of provenances ($F_{ST}$ = 0.09) was lower than the within-site provenance effects we measured for tree ring width (from 13.5 to 23.18%), suggesting a potential weak effect of natural selection on provenance ring width differences.

Our design, also, cannot formally test for local adaptation as it is not a reciprocal transplant experiment including local and foreign genotypes and sites (Kawecki & Ebert 2004). Yet, the fact that we observed significant genotype by environment interaction maybe an indication of local adaptation. The provenances from continental France and Spain (*P.n. subsp. salzmannii*) had higher growth during their first 15 years of life at Pomet, the harshest site which resembles most the ecological conditions of their place of origin. Despite the fact that growth later on becomes average or lower than average, this early growth advantage could reveal some level of local adaptation in *P.n. subsp. salzmannii* (Taïbi et al. 2016). Differences in early growth among *P. nigra* provenances have also been observed in other studies of common gardens (Wheeler et al. 1976, Wilcox & Miller 1975) and Varelides et al. (2001) hypothesized the existence of local adaptation at least for some provenances, such as the Greek provenance Thasos (*P.n. subsp. nigra*) in a Greek common garden.

Not only were provenance effects significant, their magnitude was also different in the different common gardens, suggesting a marked provenance-level phenotypic plasticity for radial growth. An average temperature increase between the coldest (Levens) and the warmest (Cestas) site of 4.9 °C and an average precipitation increase between the driest (Pomet) and the wettest (Cestas) site of 217 mm led to up to a 55% increase in provenance mean ring width. Although such variations are not uncommon in pines (e.g. Savva et al. 2008), they are quite substantial in *P. nigra* and indicate significant growth gains to be collected by carefully selecting provenances at sites where ecological conditions are optimal.
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**Conclusion and limits of the study**

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Taken together, our results suggest a weak divergent adaptation to temperature and precipitation differences in the subspecies of the European black pine and a shared sensitivity of growth to water deficit and early summer drought across subspecies and provenances, confirming early reports on different traits, from common gardens (Santini et al. 2019) or growth chambers (Thiel et al. 2012). This lack of strong differentiation for a key fitness-related trait also fits well with demographic inferences using molecular markers showing a recent, Holocene divergence of populations at continental scale in this species (Scotti-Saintagne et al. 2019). Yet, there were strong provenance effects on radial growth which could indicate provenance differences in resource acquisition or defense strategies (Esteban et al. 2012, Santini et al. 2019).

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Although based on radial growth only, and on trees specifically chosen to be without defects, our results can help at providing a typology for the subspecies and provenances of the European black pine. Whereas *P.n.* subsp. *salzmannii* never ranked first in any site for adult traits, at least one of its provenances (not always the same) performed well in most sites, particularly in the driest one. At the other end of the growth spectrum, *P.n.* subsp. *laricio* provenances never ranked last except in the driest, most Mediterranean site, while they were outperformed or equaled by *P.n.* subsp. *pallasiana* and *P.n.* subsp. *nigra* provenances in all other sites. As genotype x environment interaction is significant within subspecies, we suggest that provenance profiling rather than just subspecies profiling would probably be beneficial prior to plantation.

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With its strong phenotypic plasticity, this species of pine (like others, see Richter et al. 2012) is well adapted to a wide range of environments, both for timber production and ecological restoration. Subspecies *P.n.* subsp. *laricio* and *P.n.* subsp. *nigra* have been a popular plantation forestry choice in Europe, but our results demonstrate that some provenances of the lesser known and used (at least outside of its distribution range) *P.n.* subsp. *pallasiana* should be considered as well, both on acidic and calcareous soils. As *P. nigra* subspecies and provenances express different insect and disease susceptibilities (Perret et al. 2021, Watt et al. 2009), using a mixture of provenances from these subspecies in the highest fertility sites would probably be the safest plantation method both for timber production and ecological restoration outside the
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natural range of the species (Candido-Ribeiro & Aitken 2024), including in an assisted migration context (Bradley St Clair & Howe 2007). Our study also suggests not disregarding *P.n.* subsp. *salzmannii* provenances for dry site mixtures, and where drought is expected to increase due to climate change during the next decades (MedECC 2020).

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Finally, our study demonstrates the importance of common gardens for forest trees (Fady & Rihm 2022). Hard to manage, expensive and long term, they are the only experimental tools capable of validating phenotypic trait adaptation and plasticity, in the era of genomics and climate change. As they age, they become a precious resource for studying growth variations across retrospectively while controlling for environmental effects. Common gardens also constitute precious ex-situ biodiversity reserves of high patrimonial value. The generation of common gardens used here was designed to select the best material for plantation forestry before global climate change was considered an issue. We suggest that a new generation of common gardens is now needed for this high phenotypic plasticity forest tree species, with wide-ranging testing of new genotypes across contrasted environments, including at the early seedling stage, as suggested for other Mediterranean forest tree species (Ramírez-Valiente et al. 2022). We also suggest, in view of the strong genotype x environment found here, that countries protect their native local resources both in situ and as ex-situ conservation plantations (Scotti Saintagne et al. 2023).

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## Data, script and code availability

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Data and their metadata are available open access at the following address: https://doi.org/10.57745/SKPSYI. See Fady et al. (2024) in the References section.

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## Acknowledgements

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We thank the following people for their help for wood core sample collection and trait measurements: O. Gilg, F. Rei, N. Turion, D. Vauthier (INRAE UEFM, Avignon, France), L. Severin, N. Cheval, L. Puzos, N. Morrisson, L. Moras, C. Magnin (INRAE UEFP, Pierroton, France), F. Bonne, T. Paul and V. Rousselet (INRAE SILVA, Nancy, France). We thank W. Brunetto (INRAE URFM, Avignon, France), C. Berguet and M. Guillouard (Aix-Marseille Université, IMBE, France) for wood core sample preparation and treatment.
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Funding

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We acknowledge the financial support of the ANR project "AMTools" (ANR-11-AGRO-0005) to BF and of Aix-Marseille Université (Ecole Doctorale EDSE) to GG.

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Conflict of interest disclosure

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The authors declare they have no conflict of interest relating to the content of this article.

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