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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Genetic and morphological differentiation in <italic>Populus nigra</italic> L.: isolation by colonization or isolation by adaptation?</title><author><name sortKey="Dewoody, Jennifer" sort="Dewoody, Jennifer" uniqKey="Dewoody J" first="Jennifer" last="Dewoody">Jennifer Dewoody</name></author><author><name sortKey="Trewin, Harriet" sort="Trewin, Harriet" uniqKey="Trewin H" first="Harriet" last="Trewin">Harriet Trewin</name></author><author><name sortKey="Taylor, Gail" sort="Taylor, Gail" uniqKey="Taylor G" first="Gail" last="Taylor">Gail Taylor</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25857321</idno><idno type="pmc">4692097</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4692097</idno><idno type="RBID">PMC:4692097</idno><idno type="doi">10.1111/mec.13192</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000014</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000014</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Genetic and morphological differentiation in <italic>Populus nigra</italic> L.: isolation by colonization or isolation by adaptation?</title><author><name sortKey="Dewoody, Jennifer" sort="Dewoody, Jennifer" uniqKey="Dewoody J" first="Jennifer" last="Dewoody">Jennifer Dewoody</name></author><author><name sortKey="Trewin, Harriet" sort="Trewin, Harriet" uniqKey="Trewin H" first="Harriet" last="Trewin">Harriet Trewin</name></author><author><name sortKey="Taylor, Gail" sort="Taylor, Gail" uniqKey="Taylor G" first="Gail" last="Taylor">Gail Taylor</name></author></analytic><series><title level="j">Molecular Ecology</title><idno type="ISSN">0962-1083</idno><idno type="eISSN">1365-294X</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Identifying processes underlying the genetic and morphological differences among populations is a central question of evolutionary biology. Forest trees typically contain high levels of neutral genetic variation, and genetic differences are often correlated with geographic distance between populations [isolation by distance (IBD)] or are due to historic vicariance events [isolation by colonization (IBC)]. In contrast, morphological differences are largely due to local adaptation. Here, we examined genetic (microsatellite) and morphological (from a common garden experiment) variation in <italic>Populus nigra</italic> L., European black poplar, collected from 13 sites across western Europe and grown in a common garden in Belgium. Significant genetic differentiation was observed, with populations from France displaying greater admixture than the distinct Spanish and central European gene pools, consistent with previously described glacial refugia (IBC). Many quantitative traits displayed a bimodal distribution, approximately corresponding to small-leaf and large-leaf ecotypes. Examination of nine climatic variables revealed the sampling locations to have diverse climates, and although the correlation between morphological and climatic differences was significant, the pattern was not consistent with strict local adaptation. Partial Mantel tests based on multivariate summary statistics identified significant residual correlation in comparisons of small-leaf to large-leaf ecotypes, and within the small-leaf samples, but not within large-leaf ecotypes, indicating that variation within the small-leaf morphotype in particular may be adaptive. Some small-leaf populations experience climates very similar to those in large-leaf sites. We conclude that adaptive differentiation and persistent IBC acted in combination to produce the genetic and morphological patterns observed in <italic>P. nigra</italic>.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Antonovics, J" uniqKey="Antonovics J">J Antonovics</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Blenkinsop, S" uniqKey="Blenkinsop S">S Blenkinsop</name></author><author><name sortKey="Fowler, Hj" uniqKey="Fowler H">HJ Fowler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bock, Dg" uniqKey="Bock D">DG Bock</name></author><author><name sortKey="Andrew, Rl" uniqKey="Andrew R">RL Andrew</name></author><author><name sortKey="Rieseberg, L" uniqKey="Rieseberg L">L Rieseberg</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brown, Ahd" uniqKey="Brown A">AHD Brown</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cavers, S" uniqKey="Cavers S">S Cavers</name></author><author><name sortKey="Navarro, C" uniqKey="Navarro C">C Navarro</name></author><author><name sortKey="Lowe, Aj" uniqKey="Lowe A">AJ Lowe</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cottrell, Je" uniqKey="Cottrell J">JE Cottrell</name></author><author><name sortKey="Krystufek, V" uniqKey="Krystufek V">V Krystufek</name></author><author><name sortKey="Tabbener, He" uniqKey="Tabbener H">HE Tabbener</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="De Kort, H" uniqKey="De Kort H">H De Kort</name></author><author><name sortKey="Vandepitte, K" uniqKey="Vandepitte K">K Vandepitte</name></author><author><name sortKey="Bruun, Hh" uniqKey="Bruun H">HH Bruun</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dennison, Md" uniqKey="Dennison M">MD Dennison</name></author><author><name sortKey="Baker, Aj" uniqKey="Baker A">AJ Baker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dewoody, J" uniqKey="Dewoody J">J DeWoody</name></author><author><name sortKey="Nason, Jd" uniqKey="Nason J">JD Nason</name></author><author><name sortKey="Hipkins, Vd" uniqKey="Hipkins V">VD Hipkins</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dudley, Sa" uniqKey="Dudley S">SA Dudley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dudley, Sa" uniqKey="Dudley S">SA Dudley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Duminil, J" uniqKey="Duminil J">J Duminil</name></author><author><name sortKey="Fineschi, S" uniqKey="Fineschi S">S Fineschi</name></author><author><name sortKey="Hampe, A" uniqKey="Hampe A">A Hampe</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Earl, Da" uniqKey="Earl D">DA Earl</name></author><author><name sortKey="Vonholdt, Bm" uniqKey="Vonholdt B">BM vonHoldt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Eckert, Cg" uniqKey="Eckert C">CG Eckert</name></author><author><name sortKey="Manicacci, D" uniqKey="Manicacci D">D Manicacci</name></author><author><name sortKey="Barrett, Sch" uniqKey="Barrett S">SCH Barrett</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Evanno, G" uniqKey="Evanno G">G Evanno</name></author><author><name sortKey="Regnaut, S" uniqKey="Regnaut S">S Regnaut</name></author><author><name sortKey="Goudet, J" uniqKey="Goudet J">J Goudet</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fabbrini, F" uniqKey="Fabbrini F">F Fabbrini</name></author><author><name sortKey="Gaudet, M" uniqKey="Gaudet M">M Gaudet</name></author><author><name sortKey="Bastien, C" uniqKey="Bastien C">C Bastien</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Falush, D" uniqKey="Falush D">D Falush</name></author><author><name sortKey="Stephens, M" uniqKey="Stephens M">M Stephens</name></author><author><name sortKey="Pritchard, Jk" uniqKey="Pritchard J">JK Pritchard</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fossati, T" uniqKey="Fossati T">T Fossati</name></author><author><name sortKey="Grassi, F" uniqKey="Grassi F">F Grassi</name></author><author><name sortKey="Sala, F" uniqKey="Sala F">F Sala</name></author><author><name sortKey="Castiglione, S" uniqKey="Castiglione S">S Castiglione</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gailing, O" uniqKey="Gailing O">O Gailing</name></author><author><name sortKey="Lind, J" uniqKey="Lind J">J Lind</name></author><author><name sortKey="Lilleskov, E" uniqKey="Lilleskov E">E Lilleskov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gessler, A" uniqKey="Gessler A">A Gessler</name></author><author><name sortKey="Keitel, C" uniqKey="Keitel C">C Keitel</name></author><author><name sortKey="Kreuzwieser, J" uniqKey="Kreuzwieser J">J Kreuzwieser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hall, D" uniqKey="Hall D">D Hall</name></author><author><name sortKey="Luquez, V" uniqKey="Luquez V">V Luquez</name></author><author><name sortKey="Garcia, Vm" uniqKey="Garcia V">VM Garcia</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hamrick, Jl" uniqKey="Hamrick J">JL Hamrick</name></author><author><name sortKey="Godt, Mjw" uniqKey="Godt M">MJW Godt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hijmans, Rj" uniqKey="Hijmans R">RJ Hijmans</name></author><author><name sortKey="Cameron, Se" uniqKey="Cameron S">SE Cameron</name></author><author><name sortKey="Parra, Jl" uniqKey="Parra J">JL Parra</name></author><author><name sortKey="Jones, Pg" uniqKey="Jones P">PG Jones</name></author><author><name sortKey="Jarvis, A" uniqKey="Jarvis A">A Jarvis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hu, X S" uniqKey="Hu X">X-S Hu</name></author><author><name sortKey="He, F" uniqKey="He F">F He</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jensen, Jl" uniqKey="Jensen J">JL Jensen</name></author><author><name sortKey="Bohonak, Aj" uniqKey="Bohonak A">AJ Bohonak</name></author><author><name sortKey="Kelley, St" uniqKey="Kelley S">ST Kelley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kawecki, Tj" uniqKey="Kawecki T">TJ Kawecki</name></author><author><name sortKey="Evert, D" uniqKey="Evert D">D Evert</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kelly, Ck" uniqKey="Kelly C">CK Kelly</name></author><author><name sortKey="Chase, Mw" uniqKey="Chase M">MW Chase</name></author><author><name sortKey="De Bruijn, A" uniqKey="De Bruijn A">A De Bruijn</name></author><author><name sortKey="Fay, Mf" uniqKey="Fay M">MF Fay</name></author><author><name sortKey="Woodward, Fi" uniqKey="Woodward F">FI Woodward</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kremer, A" uniqKey="Kremer A">A Kremer</name></author><author><name sortKey="Kleinschmit, J" uniqKey="Kleinschmit J">J Kleinschmit</name></author><author><name sortKey="Cottrell, J" uniqKey="Cottrell J">J Cottrell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kremer, A" uniqKey="Kremer A">A Kremer</name></author><author><name sortKey="Ronce, O" uniqKey="Ronce O">O Ronce</name></author><author><name sortKey="Robledo Arnuncio, Jj" uniqKey="Robledo Arnuncio J">JJ Robledo-Arnuncio</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lecorre, V" uniqKey="Lecorre V">V LeCorre</name></author><author><name sortKey="Kremer, A" uniqKey="Kremer A">A Kremer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Leinonen, T" uniqKey="Leinonen T">T Leinonen</name></author><author><name sortKey="Mccairns, Rjs" uniqKey="Mccairns R">RJS McCairns</name></author><author><name sortKey="O Hara, Rb" uniqKey="O Hara R">RB O'Hara</name></author><author><name sortKey="Merila, J" uniqKey="Merila J">J Merila</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Loveless, Md" uniqKey="Loveless M">MD Loveless</name></author><author><name sortKey="Hamrick, Jl" uniqKey="Hamrick J">JL Hamrick</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Luikart, G" uniqKey="Luikart G">G Luikart</name></author><author><name sortKey="Cornuet, J M" uniqKey="Cornuet J">J-M Cornuet</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Luikart, G" uniqKey="Luikart G">G Luikart</name></author><author><name sortKey="Sherwin, Wb" uniqKey="Sherwin W">WB Sherwin</name></author><author><name sortKey="Steele, Bm" uniqKey="Steele B">BM Steele</name></author><author><name sortKey="Allendorf, Fw" uniqKey="Allendorf F">FW Allendorf</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Manly, Bfj" uniqKey="Manly B">BFJ Manly</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mckay, Jk" uniqKey="Mckay J">JK McKay</name></author><author><name sortKey="Latta, Rg" uniqKey="Latta R">RG Latta</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mckown, Ad" uniqKey="Mckown A">AD McKown</name></author><author><name sortKey="Guy, Rd" uniqKey="Guy R">RD Guy</name></author><author><name sortKey="Klapste, J" uniqKey="Klapste J">J Klapste</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Merila, J" uniqKey="Merila J">J Merila</name></author><author><name sortKey="Crnokrak, P" uniqKey="Crnokrak P">P Crnokrak</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mitton, Jb" uniqKey="Mitton J">JB Mitton</name></author><author><name sortKey="Duran, Kl" uniqKey="Duran K">KL Duran</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Moya Larano, J" uniqKey="Moya Larano J">J Moya-Larano</name></author><author><name sortKey="Corcobado, G" uniqKey="Corcobado G">G Corcobado</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nason, Jd" uniqKey="Nason J">JD Nason</name></author><author><name sortKey="Hamrick, Jl" uniqKey="Hamrick J">JL Hamrick</name></author><author><name sortKey="Fleming, Th" uniqKey="Fleming T">TH Fleming</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nosil, P" uniqKey="Nosil P">P Nosil</name></author><author><name sortKey="Funk, Dj" uniqKey="Funk D">DJ Funk</name></author><author><name sortKey="Ortiz Barrientos, D" uniqKey="Ortiz Barrientos D">D Ortiz-Barrientos</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ohlemuller, R" uniqKey="Ohlemuller R">R Ohlemuller</name></author><author><name sortKey="Gritti, Es" uniqKey="Gritti E">ES Gritti</name></author><author><name sortKey="Sykes, Mt" uniqKey="Sykes M">MT Sykes</name></author><author><name sortKey="Thomas, Cd" uniqKey="Thomas C">CD Thomas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Van Oosterhout, C" uniqKey="Van Oosterhout C">C van Oosterhout</name></author><author><name sortKey="Hutchinson, Wf" uniqKey="Hutchinson W">WF Hutchinson</name></author><author><name sortKey="Willis, Dpm" uniqKey="Willis D">DPM Willis</name></author><author><name sortKey="Shipley, P" uniqKey="Shipley P">P Shipley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Orsini, L" uniqKey="Orsini L">L Orsini</name></author><author><name sortKey="Corander, J" uniqKey="Corander J">J Corander</name></author><author><name sortKey="Alasentie, A" uniqKey="Alasentie A">A Alasentie</name></author><author><name sortKey="Hanski, I" uniqKey="Hanski I">I Hanski</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Orsini, L" uniqKey="Orsini L">L Orsini</name></author><author><name sortKey="Vanoverbeke, J" uniqKey="Vanoverbeke J">J Vanoverbeke</name></author><author><name sortKey="Swillen, I" uniqKey="Swillen I">I Swillen</name></author><author><name sortKey="Mergeay, J" uniqKey="Mergeay J">J Mergeay</name></author><author><name sortKey="De Meester, L" uniqKey="De Meester L">L De Meester</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Palme, Ae" uniqKey="Palme A">AE Palme</name></author><author><name sortKey="Su, Q" uniqKey="Su Q">Q Su</name></author><author><name sortKey="Rautenberg, A" uniqKey="Rautenberg A">A Rautenberg</name></author><author><name sortKey="Manni, F" uniqKey="Manni F">F Manni</name></author><author><name sortKey="Lascoux, M" uniqKey="Lascoux M">M Lascoux</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Peakall, R" uniqKey="Peakall R">R Peakall</name></author><author><name sortKey="Smouse, Pe" uniqKey="Smouse P">PE Smouse</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Peakall, R" uniqKey="Peakall R">R Peakall</name></author><author><name sortKey="Smouse, Pe" uniqKey="Smouse P">PE Smouse</name></author><author><name sortKey="Huff, Dr" uniqKey="Huff D">DR Huff</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Penuelas, J" uniqKey="Penuelas J">J Penuelas</name></author><author><name sortKey="Prieto, P" uniqKey="Prieto P">P Prieto</name></author><author><name sortKey="Beier, C" uniqKey="Beier C">C Beier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Petit, Rj" uniqKey="Petit R">RJ Petit</name></author><author><name sortKey="Csaikl, Um" uniqKey="Csaikl U">UM Csaikl</name></author><author><name sortKey="Bordacs, S" uniqKey="Bordacs S">S Bordacs</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Petit, Rj" uniqKey="Petit R">RJ Petit</name></author><author><name sortKey="Aguinagalde, I" uniqKey="Aguinagalde I">I Aguinagalde</name></author><author><name sortKey="De Beaulieu, Jl" uniqKey="De Beaulieu J">JL de Beaulieu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Picotte, J" uniqKey="Picotte J">J Picotte</name></author><author><name sortKey="Rosenthal, D" uniqKey="Rosenthal D">D Rosenthal</name></author><author><name sortKey="Rhode, J" uniqKey="Rhode J">J Rhode</name></author><author><name sortKey="Cruzan, M" uniqKey="Cruzan M">M Cruzan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Poorter, H" uniqKey="Poorter H">H Poorter</name></author><author><name sortKey="Niinemets, U" uniqKey="Niinemets U">Ü Niinemets</name></author><author><name sortKey="Poorter, L" uniqKey="Poorter L">L Poorter</name></author><author><name sortKey="Wright, Ij" uniqKey="Wright I">IJ Wright</name></author><author><name sortKey="Villar, R" uniqKey="Villar R">R Villar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pritchard, Jk" uniqKey="Pritchard J">JK Pritchard</name></author><author><name sortKey="Stephens, M" uniqKey="Stephens M">M Stephens</name></author><author><name sortKey="Donnelley, P" uniqKey="Donnelley P">P Donnelley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Raible, Cc" uniqKey="Raible C">CC Raible</name></author><author><name sortKey="Casty, C" uniqKey="Casty C">C Casty</name></author><author><name sortKey="Luterbacher, J" uniqKey="Luterbacher J">J Luterbacher</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rohde, A" uniqKey="Rohde A">A Rohde</name></author><author><name sortKey="Storme, V" uniqKey="Storme V">V Storme</name></author><author><name sortKey="Jorge, V" uniqKey="Jorge V">V Jorge</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rousset, F" uniqKey="Rousset F">F Rousset</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Royer, Dl" uniqKey="Royer D">DL Royer</name></author><author><name sortKey="Mcelwain, Jc" uniqKey="Mcelwain J">JC McElwain</name></author><author><name sortKey="Adams, Jm" uniqKey="Adams J">JM Adams</name></author><author><name sortKey="Wilf, P" uniqKey="Wilf P">P Wilf</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Salmela, Mj" uniqKey="Salmela M">MJ Salmela</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Savolainen, O" uniqKey="Savolainen O">O Savolainen</name></author><author><name sortKey="Pyhajarvi, T" uniqKey="Pyhajarvi T">T Pyhajarvi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Savolainen, O" uniqKey="Savolainen O">O Savolainen</name></author><author><name sortKey="Lascoux, M" uniqKey="Lascoux M">M Lascoux</name></author><author><name sortKey="Merlia, J" uniqKey="Merlia J">J Merlia</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Slatkin, M" uniqKey="Slatkin M">M Slatkin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smouse, Pe" uniqKey="Smouse P">PE Smouse</name></author><author><name sortKey="Peakall, R" uniqKey="Peakall R">R Peakall</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smouse, Pe" uniqKey="Smouse P">PE Smouse</name></author><author><name sortKey="Long, Jc" uniqKey="Long J">JC Long</name></author><author><name sortKey="Sokal, Rr" uniqKey="Sokal R">RR Sokal</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smulders, Mjm" uniqKey="Smulders M">MJM Smulders</name></author><author><name sortKey="Van Der Schoot, J" uniqKey="Van Der Schoot J">J van der Schoot</name></author><author><name sortKey="Arens, P" uniqKey="Arens P">P Arens</name></author><author><name sortKey="Vosman, B" uniqKey="Vosman B">B Vosman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smulders, Mjm" uniqKey="Smulders M">MJM Smulders</name></author><author><name sortKey="Cottrell, Je" uniqKey="Cottrell J">JE Cottrell</name></author><author><name sortKey="Lefevre, F" uniqKey="Lefevre F">F Lefevre</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sork, Vl" uniqKey="Sork V">VL Sork</name></author><author><name sortKey="Davis, Fw" uniqKey="Davis F">FW Davis</name></author><author><name sortKey="Westfall, R" uniqKey="Westfall R">R Westfall</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Spurgin, Lg" uniqKey="Spurgin L">LG Spurgin</name></author><author><name sortKey="Illera, Jc" uniqKey="Illera J">JC Illera</name></author><author><name sortKey="Jorgensen, Th" uniqKey="Jorgensen T">TH Jorgensen</name></author><author><name sortKey="Dawson, Da" uniqKey="Dawson D">DA Dawson</name></author><author><name sortKey="Richardson, Ds" uniqKey="Richardson D">DS Richardson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Steane, D" uniqKey="Steane D">D Steane</name></author><author><name sortKey="Conod, N" uniqKey="Conod N">N Conod</name></author><author><name sortKey="Jones, R" uniqKey="Jones R">R Jones</name></author><author><name sortKey="Vaillancourt, R" uniqKey="Vaillancourt R">R Vaillancourt</name></author><author><name sortKey="Potts, B" uniqKey="Potts B">B Potts</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Turesson, G" uniqKey="Turesson G">G Turesson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tzedakis, Pc" uniqKey="Tzedakis P">PC Tzedakis</name></author><author><name sortKey="Emerson, Bc" uniqKey="Emerson B">BC Emerson</name></author><author><name sortKey="Hewitt, Gm" uniqKey="Hewitt G">GM Hewitt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vendramin, Gg" uniqKey="Vendramin G">GG Vendramin</name></author><author><name sortKey="Anzidei, M" uniqKey="Anzidei M">M Anzidei</name></author><author><name sortKey="Madaghiele, A" uniqKey="Madaghiele A">A Madaghiele</name></author><author><name sortKey="Sperisen, C" uniqKey="Sperisen C">C Sperisen</name></author><author><name sortKey="Bucci, G" uniqKey="Bucci G">G Bucci</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Viger, M" uniqKey="Viger M">M Viger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Westoby, M" uniqKey="Westoby M">M Westoby</name></author><author><name sortKey="Wright, Ij" uniqKey="Wright I">IJ Wright</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wright, S" uniqKey="Wright S">S Wright</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yang, X D" uniqKey="Yang X">X-D Yang</name></author><author><name sortKey="Yan, E R" uniqKey="Yan E">E-R Yan</name></author><author><name sortKey="Chang, Sx" uniqKey="Chang S">SX Chang</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mol Ecol</journal-id><journal-id journal-id-type="iso-abbrev">Mol. Ecol</journal-id><journal-id journal-id-type="publisher-id">mec</journal-id><journal-title-group><journal-title>Molecular Ecology</journal-title></journal-title-group><issn pub-type="ppub">0962-1083</issn><issn pub-type="epub">1365-294X</issn><publisher><publisher-name>Blackwell Publishing Ltd</publisher-name><publisher-loc>Oxford, UK</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25857321</article-id><article-id pub-id-type="pmc">4692097</article-id><article-id pub-id-type="doi">10.1111/mec.13192</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Articles</subject></subj-group></article-categories><title-group><article-title>Genetic and morphological differentiation in <italic>Populus nigra</italic> L.: isolation by colonization or isolation by adaptation?</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>DeWoody</surname><given-names>Jennifer</given-names></name><xref ref-type="author-notes" rid="fn1">1</xref></contrib><contrib contrib-type="author"><name><surname>Trewin</surname><given-names>Harriet</given-names></name><xref ref-type="author-notes" rid="fn2">2</xref></contrib><contrib contrib-type="author"><name><surname>Taylor</surname><given-names>Gail</given-names></name></contrib><aff><institution>Centre for Life Sciences, Unviersity of Southampton</institution><addr-line>Building 85, Highfield Campus, Southampton, SO17 1BJ, UK</addr-line></aff></contrib-group><author-notes><corresp id="cor1">Gail Taylor, Fax: +44 23 8059 5159; E-mail: <email>g.taylor@soton.ac.uk</email></corresp><fn id="fn1" fn-type="present-address"><label>1</label><p>Present address: USDA Forest Service, National Forest Genetics Lab, 2480 Carson Road, Placerville, CA 95667, USA</p></fn><fn id="fn2" fn-type="present-address"><label>2</label><p>Present address: Biotechnology & Biological Sciences Research Council, Polaris House, North Star Avenue, Swindon, Wiltshire, SN2 IUH, UK</p></fn><fn><p>The copyright line for this article was changed on 18 August, 2015 after original online publication.</p></fn><fn><p>G.T. and J.D. conceived and designed the experiment; H.T. collected morphological data; and J.D. collected genetic data, conducted analyses and drafted the manuscript.</p></fn></author-notes><pub-date pub-type="ppub"><month>6</month><year>2015</year></pub-date><pub-date pub-type="epub"><day>14</day><month>5</month><year>2015</year></pub-date><volume>24</volume><issue>11</issue><fpage>2641</fpage><lpage>2655</lpage><history><date date-type="received"><day>10</day><month>1</month><year>2014</year></date><date date-type="rev-recd"><day>26</day><month>3</month><year>2015</year></date><date date-type="accepted"><day>02</day><month>4</month><year>2015</year></date></history><permissions><copyright-statement>© 2015 The Authors. <italic>Molecular Ecology</italic> Published by John Wiley & Sons Ltd.</copyright-statement><copyright-year>2015</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>Identifying processes underlying the genetic and morphological differences among populations is a central question of evolutionary biology. Forest trees typically contain high levels of neutral genetic variation, and genetic differences are often correlated with geographic distance between populations [isolation by distance (IBD)] or are due to historic vicariance events [isolation by colonization (IBC)]. In contrast, morphological differences are largely due to local adaptation. Here, we examined genetic (microsatellite) and morphological (from a common garden experiment) variation in <italic>Populus nigra</italic> L., European black poplar, collected from 13 sites across western Europe and grown in a common garden in Belgium. Significant genetic differentiation was observed, with populations from France displaying greater admixture than the distinct Spanish and central European gene pools, consistent with previously described glacial refugia (IBC). Many quantitative traits displayed a bimodal distribution, approximately corresponding to small-leaf and large-leaf ecotypes. Examination of nine climatic variables revealed the sampling locations to have diverse climates, and although the correlation between morphological and climatic differences was significant, the pattern was not consistent with strict local adaptation. Partial Mantel tests based on multivariate summary statistics identified significant residual correlation in comparisons of small-leaf to large-leaf ecotypes, and within the small-leaf samples, but not within large-leaf ecotypes, indicating that variation within the small-leaf morphotype in particular may be adaptive. Some small-leaf populations experience climates very similar to those in large-leaf sites. We conclude that adaptive differentiation and persistent IBC acted in combination to produce the genetic and morphological patterns observed in <italic>P. nigra</italic>.</p></abstract><kwd-group><kwd>biomass</kwd><kwd>common garden experiment</kwd><kwd>European black poplar</kwd><kwd>leaf size</kwd><kwd>microsatellites</kwd></kwd-group></article-meta></front><body><sec><title>Introduction</title><p>Identifying the evolutionary processes controlling genetic structure and morphological diversity is a central aim of evolutionary biology. The genetic structures of species have been examined using putatively neutral genetic markers for decades (Brown <xref rid="b4" ref-type="bibr">1978</xref>; Loveless & Hamrick <xref rid="b31" ref-type="bibr">1984</xref>; Hamrick & Godt <xref rid="b21" ref-type="bibr">1996</xref>). Genetic differentiation at neutral markers is typically driven by gene flow between populations, genetic drift and mutation of novel alleles (Wright <xref rid="b75" ref-type="bibr">1931</xref>). Natural selection is not expected to act on neutral markers; thus, genetic structure should reflect demographic histories, that is the level of inbreeding and migration within and among populations. In plant species, the mating system and dispersal mechanism have significant effects on the levels of genetic differentiation observed among populations (Loveless & Hamrick <xref rid="b31" ref-type="bibr">1984</xref>; Duminil <italic>et al</italic>. <xref rid="b12" ref-type="bibr">2007</xref>). Historic vicariance events may also affect the distribution of genetic variation, especially in longer-lived species (Nason <italic>et al</italic>. <xref rid="b40" ref-type="bibr">2002</xref>; Petit <italic>et al</italic>. <xref rid="b51" ref-type="bibr">2003</xref>; Savolainen & Pyhajarvi <xref rid="b60" ref-type="bibr">2007</xref>).</p><p>Plant morphology, in contrast, is widely considered adaptive (Turesson <xref rid="b70" ref-type="bibr">1922</xref>; Westoby & Wright <xref rid="b74" ref-type="bibr">2006</xref>). Phenotypic differentiation among populations reflects a balance between natural selection in the local environment, migration of alleles via gene flow (Antonovics <xref rid="b1" ref-type="bibr">1968</xref>) and, at a lower frequency, the acquisition of novel traits through mutation. Natural selection within a population must be strong enough to overcome gene flow from morphologically divergent populations in order to maintain phenotypic differentiation (Kremer <italic>et al</italic>. <xref rid="b28" ref-type="bibr">2012</xref>). The ever-increasing literature comparing differentiation in morphological traits and that at neutral marker loci indicate that phenotypic differentiation is typically greater than neutral genetic differentiation, implying natural selection overcomes ongoing gene flow to maintain morphological differences (Merila & Crnokrak <xref rid="b37" ref-type="bibr">2001</xref>; McKay & Latta <xref rid="b35" ref-type="bibr">2002</xref>; Cavers <italic>et al</italic>. <xref rid="b5" ref-type="bibr">2004</xref>; Steane <italic>et al</italic>. <xref rid="b69" ref-type="bibr">2006</xref>; Hall <italic>et al</italic>. <xref rid="b20" ref-type="bibr">2007</xref>; Leinonen <italic>et al</italic>. <xref rid="b30" ref-type="bibr">2013</xref>).</p><p>The consequences of these adaptive and neutral processes are not mutually exclusive, and natural populations are expected to experience them in combination (Cavers <italic>et al</italic>. <xref rid="b5" ref-type="bibr">2004</xref>; Orsini <italic>et al</italic>. <xref rid="b45" ref-type="bibr">2013</xref>). Divergent phenotypic selection may drive genetic differentiation at neutral loci (Nosil <italic>et al</italic>. <xref rid="b41" ref-type="bibr">2009</xref>). Significant structure is expected at neutral loci if selection is sufficient to reduce the fitness of maladapted migrants (LeCorre & Kremer <xref rid="b29" ref-type="bibr">2003</xref>; Nosil <italic>et al</italic>. <xref rid="b41" ref-type="bibr">2009</xref>). Over generations, multilocus genotypes at neutral loci may become differentiated as a result of selective pressures. While correlations between allele frequencies and environment have been reported in several plant species (e.g. Kelly <italic>et al</italic>. <xref rid="b26" ref-type="bibr">2003</xref>; Mitton & Duran <xref rid="b38" ref-type="bibr">2004</xref>; Sork <italic>et al</italic>. <xref rid="b67" ref-type="bibr">2010</xref>), isolation by adaptation (IBA), the correlation between allele frequencies and morphology while controlling for geographic separation, is rarely considered in studies across larger geographic areas. Recent literature reviews identified up to 33 studies addressing IBA in genetic differentiation, with only two focusing on tree species (Nosil <italic>et al</italic>. <xref rid="b41" ref-type="bibr">2009</xref>; Orsini <italic>et al</italic>. <xref rid="b45" ref-type="bibr">2013</xref>).</p><p>The well-established and widely tested process of isolation by distance (IBD) results in genetic differentiation increasing as a function of the geographic distance between populations (Slatkin <xref rid="b62" ref-type="bibr">1993</xref>; Rousset <xref rid="b57" ref-type="bibr">1997</xref>). That is, populations that are more distant geographically will have lower rates of gene flow, and will differentiate even in the absence of divergent selection. This contemporary IBD has recently been called isolation-by-dispersal limitation (Orsini <italic>et al</italic>. <xref rid="b45" ref-type="bibr">2013</xref>) Geographic structure may result in morphological divergence due to genetic drift alone (Dennison & Baker <xref rid="b8" ref-type="bibr">1991</xref>; Eckert <italic>et al</italic>. <xref rid="b14" ref-type="bibr">1996</xref>).</p><p>For many species, an extreme geographic isolation took place at the most recent glacial maximum (ending 15 000 years before present), which was sufficient to reduce gene flow among refugia across the Northern Hemisphere. This historic vicariance resulting from subsequent postglacial migration, called isolation by colonization (IBC), is distinct from contemporary IBD and may produce different patterns of genetic differentiation (Spurgin <italic>et al</italic>. <xref rid="b68" ref-type="bibr">2014</xref>). If contemporary levels of gene flow and the time since colonization are sufficient, the genetic signatures of IBC may be eroded, leaving no relationship between geographic distance and genetic differentiation. Serial colonization, however, is expected to produce a persistent correlation between genetic and geographic distance at both neutral and adaptive loci (Orsini <italic>et al</italic>. <xref rid="b45" ref-type="bibr">2013</xref>), even in the absence of local adaptation. Recolonization patterns following glacial melting have been well described in forest trees using chloroplast markers (Kremer <italic>et al</italic>. <xref rid="b27" ref-type="bibr">2002</xref>; Petit <italic>et al</italic>. <xref rid="b50" ref-type="bibr">2002</xref>; Palme <italic>et al</italic>. <xref rid="b46" ref-type="bibr">2003</xref>; Cottrell <italic>et al</italic>. <xref rid="b6" ref-type="bibr">2005</xref>). While historic genetic signatures are well studied, morphological differentiation among recolonized populations is rarely considered a consequence of historic phenotypes of the ancestral gene pools. Rather, even in long-lived forest trees, phenotype is expected to be a consequence of local adaptation (i.e. correlate to climatic differences and not geographic distance) (Gailing <italic>et al</italic>. <xref rid="b18" ref-type="bibr">2012</xref>), and not reflect the historic differences (Kremer <italic>et al</italic>. <xref rid="b27" ref-type="bibr">2002</xref>).</p><p><italic>Populus nigra</italic> L., the European black poplar, is a riparian tree widely distributed across Europe and into Asia and northern Africa. Likely restricted to three glacial refugia in western Europe during the most recent glacial maximum (Cottrell <italic>et al</italic>. <xref rid="b6" ref-type="bibr">2005</xref>), chloroplast haplotype patterns identified two major and one minor routes taken by <italic>P. nigra</italic> in recolonizing central Europe. Populations in France were most likely colonized from the Iberian refuge, while populations in Germany, the Lowlands, and eastward into central Europe probably arose from refugia in the Italian peninsula and Balkan region. Today, <italic>P. nigra</italic> is recognized as both ecologically and economically important in Europe. As a keystone species, <italic>P. nigra</italic> colonizes newly disturbed riparian sites and provides critical habitat in these human-impacted environments. Due to the modification of major rivers across Europe and its natural patchy preferred habitat, <italic>P. nigra</italic> is restricted to isolated populations across the landscape. As a fast-growing tree, <italic>P. nigra</italic> is the focus of breeding and management programmes for wood and biofuel production aimed at identifying genetic variants involved in growth (Fabbrini <italic>et al</italic>. <xref rid="b16" ref-type="bibr">2012</xref>).</p><p>Across its range, <italic>P. nigra</italic> displays remarkable phenotypic variation. Trees from central Europe display high growth rates, large central stems and large leaf sizes, and consequently high biomass production. Black poplar trees from regions having hot and dry Mediterranean summers produce smaller leaves and a branching growth habit, likely partial adaptations to seasonal drought (Viger <xref rid="b73" ref-type="bibr">2011</xref>). A better understanding of the evolution of morphological variation and genetic structure in <italic>P. nigra</italic> will assist breeding and conservation efforts.</p><p>This study tested for correspondence between genetic structure, morphological variation and climatic differences in <italic>P. nigra</italic> genotypes sampled from 13 populations from western Europe and grown in a common garden study. We tested for IBD and IBA by comparing neutral genetic markers, phenotypic traits and climate differences between sampling sites. Genetic differentiation was examined using a panel of nine microsatellite markers, and morphological variation was assessed for 12 traits in the common garden study. We then used multivariate analyses and full and partial Mantel tests to examine the relative roles of geographic and adaptive isolation in determining the genetic structure of a keystone forest tree.</p></sec><sec sec-type="methods"><title>Materials and methods</title><sec><title>Study system and collections</title><p><italic>Populus nigra</italic> L. is restricted to riparian habitat, resulting in a patchy occurrence across the broadest landscape scale. Unlike the canonical climax forest tree species, <italic>P. nigra</italic> is fast-growing, early successional, and dioecious, with male and female flowers occurring on separate plants. Samples were collected from 13 natural populations of <italic>P. nigra</italic> from France, Germany, Italy, the Netherlands and Spain (Rohde <italic>et al</italic>. <xref rid="b56" ref-type="bibr">2011</xref>; Table <xref ref-type="table" rid="tbl1">1</xref>, Fig.<xref ref-type="fig" rid="fig01">1</xref>). To describe the environmental differences experienced by each population, a variety of meteorological data was gathered for each collection site: four measures of temperature: mean annual temperature (MATemp, °C), temperature seasonality (standard deviation ×100, SDTemp), maximum temperature of the warmest month (MaxTemp, °C) and minimum temperature of the coldest month (MinTemp, °C); four measures of precipitation: mean total annual precipitation (MAPpt, mm), precipitation seasonality (a coefficient of variation; VarPpt), precipitation of the wettest month (MaxPpt, mm) and precipitation of the driest month (MinPpt, mm); and the maximum day length on the summer solstice (MaxDay, h). Temperature and precipitation data were taken from <ext-link ext-link-type="uri" xlink:href="http://www.worldclim.org">http://www.worldclim.org</ext-link> (Hijmans <italic>et al</italic>. <xref rid="b22" ref-type="bibr">2005</xref>), a collection of data from the years 1950 to 2000. Maximum day length was from the U.S. Naval Observatory Astronomical Applications Department (<ext-link ext-link-type="uri" xlink:href="http://aa.usno.navy.mil/data/docs/RS_OneDay.php">http://aa.usno.navy.mil/data/docs/RS_OneDay.php</ext-link>) and served as a proxy for latitude.</p><table-wrap id="tbl1" position="float"><label>Table 1</label><caption><p><italic>Populus nigra</italic> populations sampled for phenotypic analysis in a common garden study</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Abbrev.</th><th align="left" rowspan="1" colspan="1">Country</th><th align="left" rowspan="1" colspan="1">Population</th><th align="left" rowspan="1" colspan="1">Latitude</th><th align="left" rowspan="1" colspan="1">Longitude</th><th align="left" rowspan="1" colspan="1"><italic>N</italic><sub>M</sub></th><th align="left" rowspan="1" colspan="1"><italic>N</italic><sub>G</sub></th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">FR1</td><td align="left" rowspan="1" colspan="1">France</td><td align="left" rowspan="1" colspan="1">Drôme 1</td><td align="left" rowspan="1" colspan="1">44.6833</td><td align="left" rowspan="1" colspan="1">5.4000</td><td align="left" rowspan="1" colspan="1">63</td><td align="left" rowspan="1" colspan="1">31</td></tr><tr><td align="left" rowspan="1" colspan="1">FR2</td><td align="left" rowspan="1" colspan="1">France</td><td align="left" rowspan="1" colspan="1">Drôme 6</td><td align="left" rowspan="1" colspan="1">44.7500</td><td align="left" rowspan="1" colspan="1">4.9167</td><td align="left" rowspan="1" colspan="1">63</td><td align="left" rowspan="1" colspan="1">45</td></tr><tr><td align="left" rowspan="1" colspan="1">FR3</td><td align="left" rowspan="1" colspan="1">France</td><td align="left" rowspan="1" colspan="1">Durance</td><td align="left" rowspan="1" colspan="1">43.7847</td><td align="left" rowspan="1" colspan="1">5.5569</td><td align="left" rowspan="1" colspan="1">12</td><td align="left" rowspan="1" colspan="1">9</td></tr><tr><td align="left" rowspan="1" colspan="1">FR4</td><td align="left" rowspan="1" colspan="1">France</td><td align="left" rowspan="1" colspan="1">Loire East</td><td align="left" rowspan="1" colspan="1">47.3295</td><td align="left" rowspan="1" colspan="1">2.9200</td><td align="left" rowspan="1" colspan="1">26</td><td align="left" rowspan="1" colspan="1">6</td></tr><tr><td align="left" rowspan="1" colspan="1">FR5</td><td align="left" rowspan="1" colspan="1">France</td><td align="left" rowspan="1" colspan="1">Loire West</td><td align="left" rowspan="1" colspan="1">47.2571</td><td align="left" rowspan="1" colspan="1">−0.5870</td><td align="left" rowspan="1" colspan="1">21</td><td align="left" rowspan="1" colspan="1">13</td></tr><tr><td align="left" rowspan="1" colspan="1">GE</td><td align="left" rowspan="1" colspan="1">Germany</td><td align="left" rowspan="1" colspan="1">Kuhkopf</td><td align="left" rowspan="1" colspan="1">49.8167</td><td align="left" rowspan="1" colspan="1">8.5000</td><td align="left" rowspan="1" colspan="1">56</td><td align="left" rowspan="1" colspan="1">44</td></tr><tr><td align="left" rowspan="1" colspan="1">IT1</td><td align="left" rowspan="1" colspan="1">Italy</td><td align="left" rowspan="1" colspan="1">La Zelata</td><td align="left" rowspan="1" colspan="1">45.2667</td><td align="left" rowspan="1" colspan="1">8.9833</td><td align="left" rowspan="1" colspan="1">63</td><td align="left" rowspan="1" colspan="1">41</td></tr><tr><td align="left" rowspan="1" colspan="1">IT2</td><td align="left" rowspan="1" colspan="1">Italy</td><td align="left" rowspan="1" colspan="1">Siro Negri wood</td><td align="left" rowspan="1" colspan="1">45.2000</td><td align="left" rowspan="1" colspan="1">9.0667</td><td align="left" rowspan="1" colspan="1">44</td><td align="left" rowspan="1" colspan="1">32</td></tr><tr><td align="left" rowspan="1" colspan="1">NE1</td><td align="left" rowspan="1" colspan="1">The Netherlands</td><td align="left" rowspan="1" colspan="1">Ijssel, Rhine</td><td align="left" rowspan="1" colspan="1">52.2250</td><td align="left" rowspan="1" colspan="1">5.9600</td><td align="left" rowspan="1" colspan="1">31</td><td align="left" rowspan="1" colspan="1">23</td></tr><tr><td align="left" rowspan="1" colspan="1">NE2</td><td align="left" rowspan="1" colspan="1">The Netherlands</td><td align="left" rowspan="1" colspan="1">Individual clones</td><td align="left" rowspan="1" colspan="1">51.3583</td><td align="left" rowspan="1" colspan="1">4.5500</td><td align="left" rowspan="1" colspan="1">7</td><td align="left" rowspan="1" colspan="1">5</td></tr><tr><td align="left" rowspan="1" colspan="1">NE3</td><td align="left" rowspan="1" colspan="1">The Netherlands</td><td align="left" rowspan="1" colspan="1">Waal, Maas</td><td align="left" rowspan="1" colspan="1">51.8194</td><td align="left" rowspan="1" colspan="1">5.0900</td><td align="left" rowspan="1" colspan="1">12</td><td align="left" rowspan="1" colspan="1">9</td></tr><tr><td align="left" rowspan="1" colspan="1">SP1</td><td align="left" rowspan="1" colspan="1">Spain</td><td align="left" rowspan="1" colspan="1">Ebro 1</td><td align="left" rowspan="1" colspan="1">41.9333</td><td align="left" rowspan="1" colspan="1">−1.3833</td><td align="left" rowspan="1" colspan="1">54</td><td align="left" rowspan="1" colspan="1">20</td></tr><tr><td align="left" rowspan="1" colspan="1">SP2</td><td align="left" rowspan="1" colspan="1">Spain</td><td align="left" rowspan="1" colspan="1">Ebro 2</td><td align="left" rowspan="1" colspan="1">41.5833</td><td align="left" rowspan="1" colspan="1">−1.000</td><td align="left" rowspan="1" colspan="1">60</td><td align="left" rowspan="1" colspan="1">30</td></tr></tbody></table><table-wrap-foot><fn><p>Latitude and longitude provided in dd.dddd.</p></fn><fn><p><italic>N</italic><sub>M</sub> = number of genets analysed for morphological traits, 512 in total.</p></fn><fn><p><italic>N</italic><sub>G</sub> = number analysed for genetic markers, 308 in total.</p></fn></table-wrap-foot></table-wrap><fig id="fig01" position="float"><label>Fig. 1</label><caption><p>(A) Locations of <italic>Populus nigra</italic> populations sampled in Spain (red), France (orange), the Netherlands (green), Germany (blue) and Italy (purple) for the common garden study. Abbreviations follow Table <xref ref-type="table" rid="tbl1">1</xref>. (B) Principal components analysis of nine climatic variables (following Table <xref ref-type="table" rid="tbl2">2</xref>) reveal heterogeneous environments at the 13 sampling locations. Red arrows and text indicate the loadings of each climate variable, while black text indicates the relative climate of each sampling site.</p></caption><graphic xlink:href="mec0024-2641-f1"></graphic></fig><p>To identify the most informative but least correlated variables from the climate data set, a principal component analysis (PCA) was conducted as a means of data reduction as implemented in the <sc>r</sc> programing language (version 3.0.2) using the package stats. The first two climate components were compared to morphological (discriminant factors) and genetic (principal coordinates) differences among populations. Correlation between climatic differences and geographic distances between populations was examined using Mantel tests as implemented in <sc>genalex</sc> v. 6 (Peakall & Smouse <xref rid="b47" ref-type="bibr">2006</xref>).</p></sec><sec><title>Microsatellite analyses: resolving neutral genetic structure</title><p>A subset of genotypes from each population (<italic>N</italic> = 308 in total) were analysed for neutral nuclear markers (Table <xref ref-type="table" rid="tbl1">1</xref>). Leaves from each genotype in the common garden experiment were sampled, flash frozen in liquid nitrogen and stored at −80 °C until processed. DNA extraction and microsatellite analyses followed standard procedures as detailed in the <xref ref-type="supplementary-material" rid="SD2">Methods S1</xref> (Supporting information). A panel of nine biparentally inherited, codominant microsatellite markers was assayed for each sample: PMGC_14, PMGC_486, PMGC_2088, PMGC_2163, PMGC_2818 and PMGC_2879, from the <italic>Populus</italic> Molecular Genetics Cooperative (<ext-link ext-link-type="uri" xlink:href="http://www.ornl.gov/sci/ipgc/ssr_resource.htm">http://www.ornl.gov/sci/ipgc/ssr_resource.htm</ext-link>); and WPMS_14, WPMS_18 and WPMS_20 (Smulders <italic>et al</italic>. <xref rid="b65" ref-type="bibr">2001</xref>).</p><p>Six standard measures of genetic diversity were assessed for each population: percentage of polymorphic loci (<italic>P</italic>), mean alleles per locus (<italic>A</italic>), effective number of alleles (<italic>A</italic><sub>e</sub>), observed (<italic>H</italic><sub>o</sub>) and expected (<italic>H</italic><sub>e</sub>) heterozygosity and the fixation index over loci (<italic>F</italic>), as implemented by GenAlEx v6 (Peakall & Smouse <xref rid="b47" ref-type="bibr">2006</xref>). The presence of null alleles was assessed using the program <sc>microchecker</sc> (van Oosterhout <italic>et al</italic>. <xref rid="b43" ref-type="bibr">2004</xref>) as described by DeWoody <italic>et al</italic>. (<xref rid="b9" ref-type="bibr">2006</xref>). Evidence of a recent genetic bottleneck was assessed for each population using the Wilcoxon sign rank test for heterozygosity excess under the two-phased model of mutation as implemented by the program <sc>bottleneck</sc> (Luikart & Cornuet <xref rid="b32" ref-type="bibr">1998</xref>; Luikart <italic>et al</italic>. <xref rid="b33" ref-type="bibr">1998</xref>). Due to insufficient sample sizes, populations FR3, NE2 and SP1 were omitted from the <sc>microchecker</sc> analysis and populations FR3, FR4 and NE2 from the <sc>bottleneck</sc> analysis. Overall genetic differentiation was quantified as <italic>Φ</italic><sub>PT</sub> through the analysis of molecular variance (<sc>amova</sc>), and as individual locus <italic>F</italic><sub>ST</sub>, as implemented by <sc>genalex</sc> v. 6 (Peakall & Smouse <xref rid="b47" ref-type="bibr">2006</xref>).</p><p>Admixture was assessed using <sc>structure</sc> v2.3.3 (Pritchard <italic>et al</italic>. <xref rid="b54" ref-type="bibr">2000</xref>; Falush <italic>et al</italic>. <xref rid="b17" ref-type="bibr">2003</xref>). The likelihood of the observed data fitting a model of <italic>K</italic> genetic groups for the set <italic>K</italic> = {1:13} was estimated over five simulation runs, using a burn-in of 50 000 followed by 500 000 replications. Correlation in allele frequencies was allowed, and the remaining parameters were set to the default values. Two methods were used to infer the most likely value of <italic>K</italic>. First, the delta-K method of (Evanno <italic>et al</italic>. <xref rid="b15" ref-type="bibr">2005</xref>) was applied using the Web-based tool <sc>structure harvester</sc> (Earl & vonHoldt <xref rid="b13" ref-type="bibr">2012</xref>). Second, the distribution of the log-likelihoods was examined for the value with the highest probability and lowest variance.</p><p>To summarize the genetic differences over multilocus microsatellite genotypes, the pairwise genetic distances among individuals (Peakall <italic>et al</italic>. <xref rid="b48" ref-type="bibr">1995</xref>; Smouse & Peakall <xref rid="b63" ref-type="bibr">1999</xref>) were subjected to a principal coordinates analysis (PCoA) based on the covariance matrix with data standardization as implemented by <sc>genalex</sc> v6 (Peakall & Smouse <xref rid="b47" ref-type="bibr">2006</xref>).</p></sec><sec><title>Phenotypic measures: quantifying differences in morphology</title><p>In the spring of 2004, a common garden was established consisting of 512 genets planted as hardwood cuttings in six replicate, randomized blocks in a plantation located near the Institute of Forestry and Game Management near Geraardsbergen, Belgium (50.77N, 3.87E). Plantings were established on a grid with 0.75 × 2.0 m spacing, surrounded by a double row of the <italic>Populus</italic> cultivar ‘Muur’ to minimize edge effects. Once established, trees were cut back in early 2005 and regrowth pruned to a single dominant stem in June 2005. Site management, carried out by the local collaborators, included mechanical weed removal and fungicide application (Rohde <italic>et al</italic>. <xref rid="b56" ref-type="bibr">2011</xref>). No irrigation or fertilizer was provided during the experiment. The number of replicates was reduced to three or four for the Spanish samples due to ramet mortality and labelling inconsistencies which were resolved using microsatellite data.</p><p>In the third year of growth (2006), each ramet of <italic>P. nigra</italic> in the common garden was examined for 12 morphological characteristics: five leaf traits, two biomass traits and five cell traits. Leaf measures included leaf area, leaf length, leaf width, leaf length:width ratio (LL_LW) and specific leaf area (SLA). Biomass traits were measured as stem height and circumference at the start of the 2006 growing season. Cellular traits were measured from epidermal imprints and included epidermal cell area (mm<sup>2</sup>), stomatal number, stomatal density (SD), stomatal index (SI) and cell number per leaf (CN). Detailed methods are provided in the <xref ref-type="supplementary-material" rid="SD2">Methods S1</xref> (Supporting information).</p><p>To explore the variation in individual morphological traits, differences among population means were tested for each trait (<italic>y</italic>) using the model <italic>y</italic> = <italic>a</italic><sub><italic>x</italic></sub> + <italic>b</italic><sub><italic>y</italic></sub> + <italic>ɛ</italic>, where <italic>a</italic><sub><italic>x</italic></sub> is the population mean, <italic>b</italic><sub><italic>y</italic></sub> is the genotype nested within each population, and <italic>ε</italic> is the error. Scores for LL_LW were arcsine-transformed, and SD were log-transformed prior to analyses. This linear mixed model was implemented over genotype means using the lme function provided in the nlme package in <sc>r</sc> (R Project for Statistical Computing, Inc.) In addition, phenotypic correlations were estimated for each pair of traits using <sc>spss</sc> (v. 15.0.0; SPSS, Inc., Chicago, IL, USA).</p><p>To assess overall morphological differentiation of <italic>P. nigra</italic> populations for use in the IBA analyses, a discriminant analysis was performed on the genotype means of each trait measure. Those factors significantly contributing to differences between populations were used to visualize overall morphological differences between individuals and populations. Discriminant analyses were implemented using the Factor Analysis and Classification Analysis functions in <sc>spss</sc> (v. 15.0.0; SPSS, Inc.).</p></sec><sec><title>Tests for IBD and IBA</title><p>Four matrices were built to describe differences between populations of <italic>P. nigra</italic>: (i) genetic differences calculated as the Euclidian distance between the population means for the first two coordinates of the PCoA, (ii) morphological differences assessed as the Euclidian distance between the population means for the first two factors of the discriminant classification analysis, (iii) climate differences calculated as the Euclidian distance between the population means for the two climatic variables from the PCA and (iv) geographic distance from the latitude and longitude of the site of sample collection. To assess IBD, IBA and infer IBC, each response matrix (genetic and morphological differences) were compared to the two predictor matrices (climate differences and geographic distance) using simple Mantel tests (Smouse <italic>et al</italic>. <xref rid="b64" ref-type="bibr">1986</xref>; Manly <xref rid="b34" ref-type="bibr">1997</xref>). The simple Mantel tests were performed in <sc>genalex</sc> v. 6 (Peakall & Smouse <xref rid="b47" ref-type="bibr">2006</xref>), with significance determined via permutation tests.</p><p>To test for IBA directly, correspondence between pairwise genetic, morphological and geographic distances was assessed using partial Mantel tests The first tested for IBD as the correlation between genetic and geographic differences when controlling for morphological differences (Gen, Geo ¦ Morpho). The second tested for IBA as the correlation between morphological and genetic differences when controlling for geographic distances (Gen, Morpho ¦ Geo). Partial Mantel tests were implemented using the Isolation by Distance Web Service v. 3.15 (Jensen <italic>et al</italic>. <xref rid="b24" ref-type="bibr">2005</xref>), with significance determined via permutation tests. Where significant IBA was observed, regression analysis was used to describe the relationship of the residual morphological values vs. the residual genetic values (the partial regression plots) for all pairs of populations, comparisons of small-leaf to small-leaf populations, large-leaf to large-leaf populations, and small-leaf to large-leaf populations (Moya-Larano & Corcobado <xref rid="b39" ref-type="bibr">2008</xref>), with significance determined using <sc>anova</sc>. All regression analyses were performed in <sc>spss</sc> v17 (SPSS, Inc.).</p></sec></sec><sec sec-type="results"><title>Results</title><sec><title>Climate differences among sampling sites</title><p>The eight climate variables and day length varied across the sampling sites (Table <xref ref-type="table" rid="tbl2">2</xref>). The principal components analysis revealed distinct climates based on the minimum temperature of the coldest month (MinTemp), the seasonality of temperature (SDTemp), mean precipitation of the wettest month (MaxPpt), and the maximum day length (MaxDay) (Fig.<xref ref-type="fig" rid="fig01">1</xref>). The first two components accounted for 84% of the variance in the data. These measures distinguished the sites in Spain, in Italy and in the Netherlands, with sites in France and Germany intermediate.</p><table-wrap id="tbl2" position="float"><label>Table 2</label><caption><p>Climatic variables at 13 sites sampled for <italic>Populus nigra</italic></p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Pop.</th><th align="left" rowspan="1" colspan="1">MAPpt</th><th align="left" rowspan="1" colspan="1">VarPpt</th><th align="left" rowspan="1" colspan="1">MaxPpt</th><th align="left" rowspan="1" colspan="1">MinPpt</th><th align="left" rowspan="1" colspan="1">MATemp</th><th align="left" rowspan="1" colspan="1">SDTemp</th><th align="left" rowspan="1" colspan="1">MaxTemp</th><th align="left" rowspan="1" colspan="1">MinTemp</th><th align="left" rowspan="1" colspan="1">MaxDay</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">FR1</td><td align="left" rowspan="1" colspan="1">890</td><td align="left" rowspan="1" colspan="1">15</td><td align="left" rowspan="1" colspan="1">83</td><td align="left" rowspan="1" colspan="1">48</td><td align="left" rowspan="1" colspan="1">10.3</td><td align="left" rowspan="1" colspan="1">6259</td><td align="left" rowspan="1" colspan="1">25.7</td><td align="left" rowspan="1" colspan="1">−2.4</td><td align="left" rowspan="1" colspan="1">15.6</td></tr><tr><td align="left" rowspan="1" colspan="1">FR2</td><td align="left" rowspan="1" colspan="1">840</td><td align="left" rowspan="1" colspan="1">20</td><td align="left" rowspan="1" colspan="1">95</td><td align="left" rowspan="1" colspan="1">41</td><td align="left" rowspan="1" colspan="1">12.4</td><td align="left" rowspan="1" colspan="1">6357</td><td align="left" rowspan="1" colspan="1">28.1</td><td align="left" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">15.6</td></tr><tr><td align="left" rowspan="1" colspan="1">FR3</td><td align="left" rowspan="1" colspan="1">688</td><td align="left" rowspan="1" colspan="1">26.4</td><td align="left" rowspan="1" colspan="1">85</td><td align="left" rowspan="1" colspan="1">23.6</td><td align="left" rowspan="1" colspan="1">12.8</td><td align="left" rowspan="1" colspan="1">5945</td><td align="left" rowspan="1" colspan="1">27.4</td><td align="left" rowspan="1" colspan="1">0.6</td><td align="left" rowspan="1" colspan="1">15.5</td></tr><tr><td align="left" rowspan="1" colspan="1">FR4</td><td align="left" rowspan="1" colspan="1">707</td><td align="left" rowspan="1" colspan="1">11.3</td><td align="left" rowspan="1" colspan="1">72</td><td align="left" rowspan="1" colspan="1">47.7</td><td align="left" rowspan="1" colspan="1">11</td><td align="left" rowspan="1" colspan="1">5708</td><td align="left" rowspan="1" colspan="1">24.8</td><td align="left" rowspan="1" colspan="1">−0.1</td><td align="left" rowspan="1" colspan="1">16</td></tr><tr><td align="left" rowspan="1" colspan="1">FR5</td><td align="left" rowspan="1" colspan="1">711</td><td align="left" rowspan="1" colspan="1">17.5</td><td align="left" rowspan="1" colspan="1">77</td><td align="left" rowspan="1" colspan="1">44.3</td><td align="left" rowspan="1" colspan="1">11.6</td><td align="left" rowspan="1" colspan="1">5145</td><td align="left" rowspan="1" colspan="1">24.4</td><td align="left" rowspan="1" colspan="1">1.6</td><td align="left" rowspan="1" colspan="1">16</td></tr><tr><td align="left" rowspan="1" colspan="1">GE</td><td align="left" rowspan="1" colspan="1">590</td><td align="left" rowspan="1" colspan="1">19</td><td align="left" rowspan="1" colspan="1">65</td><td align="left" rowspan="1" colspan="1">36.1</td><td align="left" rowspan="1" colspan="1">9.9</td><td align="left" rowspan="1" colspan="1">6525</td><td align="left" rowspan="1" colspan="1">24.5</td><td align="left" rowspan="1" colspan="1">−1.8</td><td align="left" rowspan="1" colspan="1">16.3</td></tr><tr><td align="left" rowspan="1" colspan="1">IT1</td><td align="left" rowspan="1" colspan="1">982</td><td align="left" rowspan="1" colspan="1">23</td><td align="left" rowspan="1" colspan="1">122</td><td align="left" rowspan="1" colspan="1">55</td><td align="left" rowspan="1" colspan="1">13</td><td align="left" rowspan="1" colspan="1">7248</td><td align="left" rowspan="1" colspan="1">29</td><td align="left" rowspan="1" colspan="1">−1</td><td align="left" rowspan="1" colspan="1">15.7</td></tr><tr><td align="left" rowspan="1" colspan="1">IT2</td><td align="left" rowspan="1" colspan="1">966</td><td align="left" rowspan="1" colspan="1">23</td><td align="left" rowspan="1" colspan="1">121</td><td align="left" rowspan="1" colspan="1">55</td><td align="left" rowspan="1" colspan="1">13</td><td align="left" rowspan="1" colspan="1">7296</td><td align="left" rowspan="1" colspan="1">29</td><td align="left" rowspan="1" colspan="1">−0.9</td><td align="left" rowspan="1" colspan="1">15.7</td></tr><tr><td align="left" rowspan="1" colspan="1">NE1</td><td align="left" rowspan="1" colspan="1">774</td><td align="left" rowspan="1" colspan="1">15.3</td><td align="left" rowspan="1" colspan="1">77</td><td align="left" rowspan="1" colspan="1">47.3</td><td align="left" rowspan="1" colspan="1">9.3</td><td align="left" rowspan="1" colspan="1">5451</td><td align="left" rowspan="1" colspan="1">21.4</td><td align="left" rowspan="1" colspan="1">−0.7</td><td align="left" rowspan="1" colspan="1">16.8</td></tr><tr><td align="left" rowspan="1" colspan="1">NE2</td><td align="left" rowspan="1" colspan="1">802</td><td align="left" rowspan="1" colspan="1">14.8</td><td align="left" rowspan="1" colspan="1">81</td><td align="left" rowspan="1" colspan="1">50.3</td><td align="left" rowspan="1" colspan="1">9.7</td><td align="left" rowspan="1" colspan="1">5359</td><td align="left" rowspan="1" colspan="1">21.1</td><td align="left" rowspan="1" colspan="1">0.2</td><td align="left" rowspan="1" colspan="1">16.5</td></tr><tr><td align="left" rowspan="1" colspan="1">NE3</td><td align="left" rowspan="1" colspan="1">791</td><td align="left" rowspan="1" colspan="1">14.3</td><td align="left" rowspan="1" colspan="1">77</td><td align="left" rowspan="1" colspan="1">46.9</td><td align="left" rowspan="1" colspan="1">9.5</td><td align="left" rowspan="1" colspan="1">5383</td><td align="left" rowspan="1" colspan="1">21.4</td><td align="left" rowspan="1" colspan="1">−0.3</td><td align="left" rowspan="1" colspan="1">16.7</td></tr><tr><td align="left" rowspan="1" colspan="1">SP1</td><td align="left" rowspan="1" colspan="1">439</td><td align="left" rowspan="1" colspan="1">26</td><td align="left" rowspan="1" colspan="1">56</td><td align="left" rowspan="1" colspan="1">20</td><td align="left" rowspan="1" colspan="1">14.1</td><td align="left" rowspan="1" colspan="1">6097</td><td align="left" rowspan="1" colspan="1">29.7</td><td align="left" rowspan="1" colspan="1">1.8</td><td align="left" rowspan="1" colspan="1">15.2</td></tr><tr><td align="left" rowspan="1" colspan="1">SP2</td><td align="left" rowspan="1" colspan="1">365</td><td align="left" rowspan="1" colspan="1">31</td><td align="left" rowspan="1" colspan="1">53</td><td align="left" rowspan="1" colspan="1">17</td><td align="left" rowspan="1" colspan="1">13.7</td><td align="left" rowspan="1" colspan="1">6243</td><td align="left" rowspan="1" colspan="1">29.5</td><td align="left" rowspan="1" colspan="1">1.3</td><td align="left" rowspan="1" colspan="1">15.2</td></tr></tbody></table><table-wrap-foot><fn><p>MAPpt, mean annual precipitation (mm); VarPpt, precipitation seasonality; MaxPpt, mean precipitation of the wettest month (mm); MinPpt, mean precipitation of the driest month (mm); MATemp, mean annual temperature (°C); SDTemp, seasonality of temperature; MaxTemp, maximum temperature of the warmest month (°C); MinTemp, minimum temperature of the coldest month (°C); MaxDay, maximum day length (h).</p></fn></table-wrap-foot></table-wrap></sec><sec><title>Patterns of neutral genetic structure in <italic>Populus nigra</italic></title><p>Microsatellite variation revealed high levels of polymorphism and moderate levels of allelic diversity and heterozygosity, with no evidence of allele fixation (Table <xref ref-type="table" rid="tbl3">3</xref>). Null alleles were detected in three populations at locus PMGC_2088 (IT1, freq. 0.09; NE1, freq. 0.11, NE3, freq. 0.27) and at low frequency in a single population at WPMS_14 (FR5, freq. 0.15) and WPMS_20 (IT1, freq. 0.09). Low rates of mismatches between repeated samples resulted in low error rates: 3.3% per allele or 4.6% per reaction.</p><table-wrap id="tbl3" position="float"><label>Table 3</label><caption><p>Genetic diversity (mean number of samples, mean alleles per locus, effective alleles per locus, observed and expected heterozygosity, and fixation) observed at nine microsatellite loci in 13 populations of <italic>Populus nigra</italic></p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Population</th><th align="left" rowspan="1" colspan="1"><italic>N</italic></th><th align="left" rowspan="1" colspan="1"><italic>A</italic></th><th align="left" rowspan="1" colspan="1"><italic>A</italic><sub>e</sub></th><th align="left" rowspan="1" colspan="1"><italic>H</italic><sub>o</sub></th><th align="left" rowspan="1" colspan="1"><italic>H</italic><sub>e</sub></th><th align="left" rowspan="1" colspan="1"><italic>F</italic></th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">FR1</td><td align="left" rowspan="1" colspan="1">30.2</td><td align="left" rowspan="1" colspan="1">9.2</td><td align="left" rowspan="1" colspan="1">4.9</td><td align="left" rowspan="1" colspan="1">0.774</td><td align="left" rowspan="1" colspan="1">0.770</td><td align="left" rowspan="1" colspan="1">−0.006</td></tr><tr><td align="left" rowspan="1" colspan="1">FR2</td><td align="left" rowspan="1" colspan="1">42.4</td><td align="left" rowspan="1" colspan="1">11.2</td><td align="left" rowspan="1" colspan="1">6.0</td><td align="left" rowspan="1" colspan="1">0.799</td><td align="left" rowspan="1" colspan="1">0.808</td><td align="left" rowspan="1" colspan="1">0.012</td></tr><tr><td align="left" rowspan="1" colspan="1">FR3</td><td align="left" rowspan="1" colspan="1">5.9</td><td align="left" rowspan="1" colspan="1">5.4</td><td align="left" rowspan="1" colspan="1">4.0</td><td align="left" rowspan="1" colspan="1">0.727</td><td align="left" rowspan="1" colspan="1">0.708</td><td align="left" rowspan="1" colspan="1">−0.057</td></tr><tr><td align="left" rowspan="1" colspan="1">FR4</td><td align="left" rowspan="1" colspan="1">6.0</td><td align="left" rowspan="1" colspan="1">5.9</td><td align="left" rowspan="1" colspan="1">4.2</td><td align="left" rowspan="1" colspan="1">0.796</td><td align="left" rowspan="1" colspan="1">0.736</td><td align="left" rowspan="1" colspan="1">−0.084</td></tr><tr><td align="left" rowspan="1" colspan="1">FR5</td><td align="left" rowspan="1" colspan="1">12.1</td><td align="left" rowspan="1" colspan="1">7.0</td><td align="left" rowspan="1" colspan="1">5.0</td><td align="left" rowspan="1" colspan="1">0.755</td><td align="left" rowspan="1" colspan="1">0.751</td><td align="left" rowspan="1" colspan="1">−0.012</td></tr><tr><td align="left" rowspan="1" colspan="1">GE</td><td align="left" rowspan="1" colspan="1">42.0</td><td align="left" rowspan="1" colspan="1">9.0</td><td align="left" rowspan="1" colspan="1">4.3</td><td align="left" rowspan="1" colspan="1">0.767</td><td align="left" rowspan="1" colspan="1">0.743</td><td align="left" rowspan="1" colspan="1">−0.026</td></tr><tr><td align="left" rowspan="1" colspan="1">IT1</td><td align="left" rowspan="1" colspan="1">39.0</td><td align="left" rowspan="1" colspan="1">10.7</td><td align="left" rowspan="1" colspan="1">5.6</td><td align="left" rowspan="1" colspan="1">0.787</td><td align="left" rowspan="1" colspan="1">0.797</td><td align="left" rowspan="1" colspan="1">0.019</td></tr><tr><td align="left" rowspan="1" colspan="1">IT2</td><td align="left" rowspan="1" colspan="1">30.4</td><td align="left" rowspan="1" colspan="1">9.6</td><td align="left" rowspan="1" colspan="1">6.1</td><td align="left" rowspan="1" colspan="1">0.817</td><td align="left" rowspan="1" colspan="1">0.802</td><td align="left" rowspan="1" colspan="1">−0.021</td></tr><tr><td align="left" rowspan="1" colspan="1">NE1</td><td align="left" rowspan="1" colspan="1">22.4</td><td align="left" rowspan="1" colspan="1">8.2</td><td align="left" rowspan="1" colspan="1">4.8</td><td align="left" rowspan="1" colspan="1">0.813</td><td align="left" rowspan="1" colspan="1">0.777</td><td align="left" rowspan="1" colspan="1">−0.049</td></tr><tr><td align="left" rowspan="1" colspan="1">NE2</td><td align="left" rowspan="1" colspan="1">5.0</td><td align="left" rowspan="1" colspan="1">5.2</td><td align="left" rowspan="1" colspan="1">4.2</td><td align="left" rowspan="1" colspan="1">0.867</td><td align="left" rowspan="1" colspan="1">0.749</td><td align="left" rowspan="1" colspan="1">−0.168</td></tr><tr><td align="left" rowspan="1" colspan="1">NE3</td><td align="left" rowspan="1" colspan="1">8.7</td><td align="left" rowspan="1" colspan="1">5.0</td><td align="left" rowspan="1" colspan="1">3.5</td><td align="left" rowspan="1" colspan="1">0.735</td><td align="left" rowspan="1" colspan="1">0.693</td><td align="left" rowspan="1" colspan="1">−0.054</td></tr><tr><td align="left" rowspan="1" colspan="1">SP1</td><td align="left" rowspan="1" colspan="1">15.3</td><td align="left" rowspan="1" colspan="1">6.1</td><td align="left" rowspan="1" colspan="1">4.2</td><td align="left" rowspan="1" colspan="1">0.640</td><td align="left" rowspan="1" colspan="1">0.719</td><td align="left" rowspan="1" colspan="1">0.071</td></tr><tr><td align="left" rowspan="1" colspan="1">SP2</td><td align="left" rowspan="1" colspan="1">27.6</td><td align="left" rowspan="1" colspan="1">8.4</td><td align="left" rowspan="1" colspan="1">4.8</td><td align="left" rowspan="1" colspan="1">0.734</td><td align="left" rowspan="1" colspan="1">0.738</td><td align="left" rowspan="1" colspan="1">0.005</td></tr><tr><td align="left" rowspan="1" colspan="1">Overall</td><td align="left" rowspan="1" colspan="1">22.1</td><td align="left" rowspan="1" colspan="1">7.8</td><td align="left" rowspan="1" colspan="1">4.7</td><td align="left" rowspan="1" colspan="1">0.770</td><td align="left" rowspan="1" colspan="1">0.753</td><td align="left" rowspan="1" colspan="1">−0.029</td></tr></tbody></table></table-wrap><p>Sign tests for heterozygosity excess at Hardy–Weinberg equilibrium compared to that expected at mutation–drift equilibrium was observed for populations IT1 (<italic>P</italic> < 0.01), NE3 and SP1 (<italic>P</italic> < 0.05), indicating these populations have undergone a recent population bottleneck. Results for populations NE3 and SP1 may be influenced by the small sample size in this analysis. The bottleneck in population IT1 may have contributed to increased inbreeding and homozygosity identified as possible null alleles (above).</p><p>Overall genetic differentiation was significant (<italic>Φ</italic><sub>PT</sub> = 0.120, <italic>P</italic> < 0.001), indicating gene flow among populations of <italic>P. nigra</italic> is restricted across western Europe. Per-locus estimates ranged from 0.044 to 0.118 (mean = 0.072, standard deviation = 0.021) (Supporting Information).</p><p>The number of genetic clusters (<italic>K</italic>) identified by the admixture analyses varied with the method of inference used. The <sc>structure harvester</sc> method of Evanno <italic>et al</italic>. (<xref rid="b15" ref-type="bibr">2005</xref>) identified <italic>K</italic> = 2 as most likely. Individual assignment tests over two genetic groups indicated the collections from Spain, France and Italy were distinct from trees from Germany and the Netherlands (Fig.<xref ref-type="fig" rid="fig02">2</xref>C). As experience indicates the Evanno method may be overly conservative in species with significant gene flow, to identify the mostly likely biologically meaningful value of <italic>K</italic>, direct examination of likelihood ratios indicated the tests for <italic>K</italic> = 5 genetic clusters resulted in the highest likelihood without an increase in variance (<xref ref-type="supplementary-material" rid="SD1">Fig. S1</xref>, Supporting information). Individual assignment tests to five genetic groups roughly correspond to country of origin (Fig.<xref ref-type="fig" rid="fig02">2</xref>C), with the samples from Germany and the Netherlands assigned to the same genetic cluster and samples from France displaying the greatest admixture.</p><fig id="fig02" position="float"><label>Fig. 2</label><caption><p>(A) Principal coordinates analysis of microsatellite data reveals patterns of differentiation among populations of <italic>Populus nigra</italic>. (B) Discriminant classification analysis of 12 morphological traits reveals significant geographic structuring to phenotypic variation in <italic>Populus nigra</italic>. Each point represents a single genet, with colour corresponding to country of origin. Ellipses represent the 95% confidence intervals for the population means. Population means for each data type were used for pairwise comparisons in full and partial Mantel tests. (C) Admixture analysis of microsatellite data identified two (top) or five (bottom) genetic groups. Assignment of individual trees (vertical bars) roughly corresponded to geographic origin, with samples from France displaying greater admixture. Position of abbreviations below indicates the order and extent of each population. (D) Morphological differentiation among populations is typified by variation in leaf area quantified in a common garden study. Each box-and-whisker plot represents the observed measures for each population, with the centre bar indicating the median value.</p></caption><graphic xlink:href="mec0024-2641-f2"></graphic></fig><p>The PCoA revealed overall differences to be of a smaller magnitude among individual trees than populations (Fig.<xref ref-type="fig" rid="fig02">2</xref>A). The first two components explained a cumulative total of 44.0% of the variance among individuals. Significant overlap was observed between populations.</p></sec><sec><title>Phenotypic differentiation among populations</title><p>All measures of phenotype varied significantly among populations (Table <xref ref-type="table" rid="tbl4">4</xref>). Several traits displayed bimodal distributions across the collection. For instance, leaf size was strongly bimodal, with samples from Spain and France having smaller leaves than those from Italy, Germany or the Netherlands (Fig.<xref ref-type="fig" rid="fig02">2</xref>D, <xref ref-type="supplementary-material" rid="SD3">Tables S1–S5</xref>, Supporting information).</p><table-wrap id="tbl4" position="float"><label>Table 4</label><caption><p>Morphological variation in leaf, cell and biomass traits measured in a common garden study of <italic>Populus nigra</italic> from 13 natural stands in western Europe revealed significant phenotypic variation. Discriminant factor analyses were used to reduce the multivariate data into two components for isolation by adaptation comparisons</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Trait</th><th align="left" rowspan="1" colspan="1"><italic>F</italic>-ratio</th><th align="left" rowspan="1" colspan="1"><italic>P</italic>-value</th><th align="left" rowspan="1" colspan="1">Component 1</th><th align="left" rowspan="1" colspan="1">Component 2</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Leaf area</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,499</sub> = 135.1</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.948</td><td align="left" rowspan="1" colspan="1">−0.179</td></tr><tr><td align="left" rowspan="1" colspan="1">Leaf length</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,499</sub> = 133.7</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.935</td><td align="left" rowspan="1" colspan="1">−0.178</td></tr><tr><td align="left" rowspan="1" colspan="1">Leaf width</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,499</sub> = 111.4</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.938</td><td align="left" rowspan="1" colspan="1">−0.218</td></tr><tr><td align="left" rowspan="1" colspan="1">Leaf length:width</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,493</sub> = 3.265</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.931</td><td align="left" rowspan="1" colspan="1">−0.168</td></tr><tr><td align="left" rowspan="1" colspan="1">Specific leaf area</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,467</sub> = 160.0</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.520</td><td align="left" rowspan="1" colspan="1">0.697</td></tr><tr><td align="left" rowspan="1" colspan="1">Cell area</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,453</sub> = 3.36</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.487</td><td align="left" rowspan="1" colspan="1">0.742</td></tr><tr><td align="left" rowspan="1" colspan="1">Cell number per leaf</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,451</sub> = 67.8</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.248</td><td align="left" rowspan="1" colspan="1">0.660</td></tr><tr><td align="left" rowspan="1" colspan="1">Number of stomata (abaxial)</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,498</sub> = 10.5</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.923</td><td align="left" rowspan="1" colspan="1">0.044</td></tr><tr><td align="left" rowspan="1" colspan="1">Stomatal density (abaxial)</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,489</sub> = 6.27</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">0.832</td><td align="left" rowspan="1" colspan="1">−0.205</td></tr><tr><td align="left" rowspan="1" colspan="1">Stomatal index (abaxial)</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,443</sub> = 2.659</td><td align="left" rowspan="1" colspan="1">0.0019</td><td align="left" rowspan="1" colspan="1">0.878</td><td align="left" rowspan="1" colspan="1">−0.198</td></tr><tr><td align="left" rowspan="1" colspan="1">Height (second year)</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,449</sub> = 44.7</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">−0.288</td><td align="left" rowspan="1" colspan="1">0.108</td></tr><tr><td align="left" rowspan="1" colspan="1">Circumference (third year)</td><td align="left" rowspan="1" colspan="1"><italic>F</italic><sub>12,499</sub> = 78.4</td><td align="left" rowspan="1" colspan="1"><0.0001</td><td align="left" rowspan="1" colspan="1">−0.307</td><td align="left" rowspan="1" colspan="1">−0.467</td></tr><tr><td align="left" rowspan="1" colspan="1">% variation</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">54.8</td><td align="left" rowspan="1" colspan="1">16.0</td></tr></tbody></table></table-wrap><p>Correlations between morphological measures were highly significant but varied within and among trait classes (leaf traits, cell traits and biomass traits; Supporting information). The discriminant factor analysis (DFA) was required to reduce the variation of the highly correlated phenotypic measures to a smaller number of orthogonal factors (Table <xref ref-type="table" rid="tbl4">4</xref>). The first two components of the DFA described cumulative total of 71% of the variation and revealed significant geographic patterning in morphology. Samples from Spain were morphologically distinct from those from Italy, Germany and the Netherlands, with the French populations intermediate (Fig.<xref ref-type="fig" rid="fig02">2</xref>B). Leaf area was correlated with the first factor (Table <xref ref-type="table" rid="tbl4">4</xref>), indicating that identifying collections as small leaf (Spain and France) or large leaf (Germany, Italy and the Netherlands) may represent the two general morphotypes (Viger <xref rid="b73" ref-type="bibr">2011</xref>).</p></sec><sec><title>Tests for IBD, by colonization and by adaptation</title><p>Simple Mantel test identified significant correlations between the genetic, morphological, geographic and climatic matrices distance matrices (Table <xref ref-type="table" rid="tbl5">5</xref>). Correlations were strongest between the morphological and geographic matrices (<italic>r</italic> = 0.582, <italic>P</italic> < 0.001), genetic and geographic matrices (<italic>r</italic> = 0.577, <italic>P</italic> < 0.001) and morphological and genetic matrices (<italic>r</italic> = 0.522, <italic>P</italic> < 0.001). Weaker but significant correlations were observed between the morphological and climate matrices (<italic>r</italic> = 0.406, <italic>P</italic> < 0.001) and the genetic and climate matrices (<italic>r</italic> = 0.399, <italic>P</italic> = 0.004).</p><table-wrap id="tbl5" position="float"><label>Table 5</label><caption><p>Correlations between genetic (from PCoA), morphological (from discriminant factor analysis), climatic (from principal component analysis) and geographic (km) differences among 13 populations of <italic>Populus nigra</italic> tested with simple and partial Mantel tests</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Comparison</th><th align="left" rowspan="1" colspan="1"><italic>r</italic></th><th align="left" rowspan="1" colspan="1"><italic>P</italic>-value</th></tr></thead><tbody><tr><td align="left" colspan="3" rowspan="1">Simple Mantel tests</td></tr><tr><td align="left" rowspan="1" colspan="1"> Genetic, Geographic</td><td align="left" rowspan="1" colspan="1">0.633</td><td align="left" rowspan="1" colspan="1"><0.001</td></tr><tr><td align="left" rowspan="1" colspan="1"> Genetic, Climate</td><td align="left" rowspan="1" colspan="1">0.551</td><td align="left" rowspan="1" colspan="1"><0.001</td></tr><tr><td align="left" rowspan="1" colspan="1"> Morphological, Geographic</td><td align="left" rowspan="1" colspan="1">0.582</td><td align="left" rowspan="1" colspan="1"><0.001</td></tr><tr><td align="left" rowspan="1" colspan="1"> Morphological, Climate</td><td align="left" rowspan="1" colspan="1">0.416</td><td align="left" rowspan="1" colspan="1">0.002</td></tr><tr><td align="left" rowspan="1" colspan="1"> Morphological, Genetic</td><td align="left" rowspan="1" colspan="1">0.622</td><td align="left" rowspan="1" colspan="1"><0.001</td></tr><tr><td align="left" colspan="3" rowspan="1">Partial Mantel tests</td></tr><tr><td align="left" rowspan="1" colspan="1"> Genetic, Geographic | Morphological</td><td align="left" rowspan="1" colspan="1">0.426</td><td align="left" rowspan="1" colspan="1"><0.001</td></tr><tr><td align="left" rowspan="1" colspan="1"> Genetic, Climate | Morphological</td><td align="left" rowspan="1" colspan="1">0.418</td><td align="left" rowspan="1" colspan="1">0.004</td></tr><tr><td align="left" rowspan="1" colspan="1"> Morphological | Genetic, Geographic</td><td align="left" rowspan="1" colspan="1">0.403</td><td align="left" rowspan="1" colspan="1">0.004</td></tr><tr><td align="left" rowspan="1" colspan="1"> Morphological | Genetic, Climate</td><td align="left" rowspan="1" colspan="1">0.522</td><td align="left" rowspan="1" colspan="1"><0.001</td></tr></tbody></table></table-wrap><p>Significant correlation between genetic and geographic distance, independent of morphological divergence (Gen, Geo¦Morpho), indicates that IBD has influenced the genetic structure of <italic>P. nigra</italic> in western Europe (Table <xref ref-type="table" rid="tbl5">5</xref>). Genetic differences increased as a function of distance, consistent with the genetic pattern resolved by the admixture analyses. Tests using pairwise <italic>F</italic><sub>ST</sub> (Rousset <xref rid="b57" ref-type="bibr">1997</xref>) measures and log-transformed data were significant and concordant (<xref ref-type="supplementary-material" rid="SD3">Tables S1–S5</xref>, Supporting information).</p><p>Isolation by adaptation also contributed to the genetic structure of populations, as genetic similarity increased with phenotypic similarity, even when controlling for geographic structure among populations (Gen, Morpho¦Geo). Analyses of log-transformed data were consistent (data not presented). This result indicates that genetic differentiation at microsatellite loci may be influenced by reduced gene flow between morphologically distinct populations or reflect historic vicariance due to IBC.</p><p>Examination of partial regression plots of the genetic and morphological differences between populations further revealed the putative source of IBA (Fig. <xref ref-type="fig" rid="fig04">4</xref>). IBA was significant among comparisons of all pairs of populations (<italic>F</italic><sub>1,76</sub> = 28.1, <italic>P</italic> < 0.001; slope = 0.038, 95% CI 0.023–0.052). Categorical comparisons of small-leaf and large-leaf pairs revealed the trend to be driven by differences among the small-leaf populations. Significant positive relationships were observed in small-leaf to small-leaf comparisons (<italic>F</italic><sub>1,19</sub> = 17.7, <italic>P</italic> < 0.001; slope = 0.07, 95% CI 0.035–0.105), and small-leaf to large-leaf comparisons (<italic>F</italic><sub>1,40</sub> = 26.5, <italic>P</italic> < 0.001; slope = 0.053, 95% CI 0.032–0.074), but not large-leaf to large-leaf comparisons (<italic>F</italic><sub>1,13</sub> = 3.52, <italic>P</italic> = 0.083; slope = 0.02, 95% CI −0.003–0.043). Thus, the genetic and morphological variation observed in the large-leaf populations was fully explained by IBD, with gene flow decreasing as a function of distance. However, when comparing small-leaf to small-leaf, or small-leaf to large-leaf populations, the genetic differentiation between populations resulted from IBA as well, and populations are more genetically dissimilar than their geographic distance would predict.</p></sec></sec><sec sec-type="discussion"><title>Discussion</title><p>In the strictest terms, evidence of local adaptation requires that a species displays multiple morphotypes, each having higher fitness in its native habitat than the others, as confirmed through reciprocal transplant experiments (Kawecki & Evert <xref rid="b25" ref-type="bibr">2004</xref>; Savolainen <italic>et al</italic>. <xref rid="b61" ref-type="bibr">2013</xref>). Adaptive differentiation, however, can be described by examining patterns of genetic differences and climatic variation (Sork <italic>et al</italic>. <xref rid="b67" ref-type="bibr">2010</xref>; Salmela <xref rid="b59" ref-type="bibr">2014</xref>). Our study of <italic>P. nigra</italic> revealed distinct morphological and genetic variation in trees from across western Europe and related these patterns to differences in local climate at each site. We conclude that adaptive differentiation and persistent IBC acted in combination to produce the observed genetic and morphological patterns.</p><p>Leaf size, branching architecture and growth rate are all considered adaptive traits in trees and, in particular, may be linked to water availability (Dudley <xref rid="b10" ref-type="bibr">1996a</xref>,<xref rid="b11" ref-type="bibr">b</xref>; Picotte <italic>et al</italic>. <xref rid="b52" ref-type="bibr">2007</xref>; Yang <italic>et al</italic>. <xref rid="b76" ref-type="bibr">2014</xref>). Species or morphotypes adapted to lower or seasonal precipitation tend to display smaller, thicker leaves, greater branching and slower growth rate in response to the environmental stress (Poorter <italic>et al</italic>. <xref rid="b53" ref-type="bibr">2009</xref>; De Kort <italic>et al</italic>. <xref rid="b7" ref-type="bibr">2014</xref>). In our common garden experiment, trees from Spain and France displayed small leaves, a branching architecture and smaller circumference, while trees from northern Italy, Germany and the Netherlands displayed large leaves, a straight architecture and large circumference. If these morphotypes are strictly adaptive, we would expect small-leaf trees to inhabit similar environments, and those would be distinct from climates experienced by large-leaf trees. Although the correlation between morphological difference and climatic difference was significant in <italic>P. nigra</italic> (Fig.<xref ref-type="fig" rid="fig03">3</xref>), the pattern did not reveal that different morphotypes inhabit different environments. Examination of nine climatic variables revealed the sampling locations to have diverse climates, with some climates in France (small-leaf populations) similar to the site in Germany (large-leaf), although climates in Spain (small-leaf), Italy (large-leaf) and the Netherlands (large-leaf) were all distinct (Fig.<xref ref-type="fig" rid="fig01">1</xref>).</p><fig id="fig03" position="float"><label>Fig. 3</label><caption><p>Genetic differences between populations (from PCoA, top row), allele frequency variance (<italic>F</italic><sub>ST</sub>, middle row) and morphological differences between populations (from discriminant factor analysis, bottom row) all correlate with geographic distance (left panels) more than climatic differences (right panels) between sampling sites. Note that high levels of morphological differences are observed between sites with similar climates (triangle symbols, bottom right pane). Correlations from simple Mantel tests, with significance determined using permutation tests. n.s. = <italic>P</italic>-values are nonsignificant after sequential Bonferroni corrections.</p></caption><graphic xlink:href="mec0024-2641-f3"></graphic></fig><p>Further, if selection was strong enough to reduce successful gene flow between morphotypes, we would expect residuals from the partial correlations (i.e. IBA; Nosil <italic>et al</italic>. <xref rid="b41" ref-type="bibr">2009</xref>), to be driven by comparisons of different morphotypes (e.g. small-leaf to large-leaf). The significant residual correlation in <italic>P. nigra</italic> was observed in small-leaf to large-leaf comparisons, but also in small-leaf to small-leaf comparisons, indicating that variation within the small-leaf morphotype in particular may be adaptive (Fig.<xref ref-type="fig" rid="fig04">4</xref>). For comparison, in a similar study of adaptive differentiation in <italic>Alnus</italic>, correlation between phenotypic and neutral genetic structure was significant but weak (<sub>adj</sub><italic>R</italic><sup>2</sup><sub>cum</sub> = 0.05, <italic>P</italic> < 0.001), and no evidence was observed for IBD (De Kort <italic>et al</italic>. <xref rid="b7" ref-type="bibr">2014</xref>).</p><fig id="fig04" position="float"><label>Fig. 4</label><caption><p>Partial regression plots illustrating correlated genetic and morphological differences between populations of <italic>Populus nigra</italic> after controlling for the effects of geographic distance. Points represent pairwise comparisons between two small-leaf populations (squares), two large-leaf populations (circles) or populations with differing morphology (triangles). Lines represent significant regressions of the residuals, with significance determined using <sc>anova</sc>. Comparisons of large-leaf to large-leaf populations revealed no significant relationship. Significance did not change after Bonferroni corrections.</p></caption><graphic xlink:href="mec0024-2641-f4"></graphic></fig><p>Isolation by distance and IBC due to serial recolonization have also contributed to the morphological and genetic structure of <italic>P. nigra</italic> and may explain the inconsistency between morphology and climate in the populations from France. Several tree species maintain signatures of postglacial range expansions in their extant genetic structures (Vendramin <italic>et al</italic>. <xref rid="b72" ref-type="bibr">2000</xref>; Petit <italic>et al</italic>. <xref rid="b50" ref-type="bibr">2002</xref>; Palme <italic>et al</italic>. <xref rid="b46" ref-type="bibr">2003</xref>; Tzedakis <italic>et al</italic>. <xref rid="b71" ref-type="bibr">2013</xref>), although local adaptation is expected to remove these patterns from morphological traits (Cavers <italic>et al</italic>. <xref rid="b5" ref-type="bibr">2004</xref>). For species existing as a metapopulation (<italic>P. nigra</italic> better fits a model of isolated populations requiring regular disturbance than the canonical climax forest tree), current genetic structure may reflect historic rather than extant demographic patterns (Orsini <italic>et al</italic>. <xref rid="b44" ref-type="bibr">2008</xref>), although differences between IBD and IBC are difficult to distinguish using neutral markers (Orsini <italic>et al</italic>. <xref rid="b45" ref-type="bibr">2013</xref>). If gene flow is insufficient to overcome the historic differentiation, a signature of historic vicariance may persist in the morphological differences between populations. The strongest evidence of IBC would come from comparing differences at slow-evolving or maternally inherited loci (e.g. chloroplast haplotypes), morphological differences and geographic distance. As the sole process influencing a species, IBC is expected to result in a lack of correlation between genetic differentiation and distance (IBD) or environment (IBA; Orsini <italic>et al</italic>. <xref rid="b45" ref-type="bibr">2013</xref>). Although our study lacks direct tests of postglacial migration from plastid sequences, the pattern of postglacial recolonization in <italic>P. nigra</italic> has been previously described. Cottrell <italic>et al</italic>. (<xref rid="b6" ref-type="bibr">2005</xref>) identified up to three putative refugia and demonstrated that trees in France displayed haplotypes more similar to Iberian populations than those from central Europe. These patterns of plastid variation are generally similar to the pattern of morphological variation observed in the common garden study, where small-leaf trees from Spain and France overlapped in morphology, but were generally distinct from large-leaf trees from central Europe. There are three possible explanations for the similarities in the plastid and morphological patterns: (i) the plastid variation reflects adaptive differences and thus IBA, (ii) the morphological differences maintain a residual signature of the historic vicariance from the last glacial maximum, and (iii) the patterns are similar due to the influence of a third untested process. Given the growing literature demonstrating that plastid genomes are not strictly neutral (Bock <italic>et al</italic>. <xref rid="b3" ref-type="bibr">2014</xref>), the congruence between the morphological differences and signature of recolonization described by plastid variation (Cottrell <italic>et al</italic>. <xref rid="b6" ref-type="bibr">2005</xref>) may be adaptive. As with correlations between morphology and climate, if the plastid (historic) variation mirrors the selective differentiation, we would expect plants with similar morphology to inhabit similar environments, yet the diversity of climates inhabited by small-leaf populations in France (Fig.<xref ref-type="fig" rid="fig01">1</xref>) is inconsistent with this expectation. The morphological variation in <italic>P. nigra</italic> is consistent with the patterns of postglacial recolonization reported in a number of tree species, indicating morphology may reflect, in part, IBD due to serial colonization. However, we cannot rule out the third possibility that we have failed to identify the causative process underlying these correlations. Historic and extant population structure is gaining recognition as a potential force shaping morphological variation in forest trees.</p><p>Efforts to correlate phenotypic variation and specific climatic variables have met with mixed success. Phenological traits tend to vary with latitude or maximum day length of the origin site, consistent with strong selective pressure from growing season length on tree species (Hall <italic>et al</italic>. <xref rid="b20" ref-type="bibr">2007</xref>; Rohde <italic>et al</italic>. <xref rid="b56" ref-type="bibr">2011</xref>; De Kort <italic>et al</italic>. <xref rid="b7" ref-type="bibr">2014</xref>; McKown <italic>et al</italic>. <xref rid="b36" ref-type="bibr">2014</xref>). Evidence of phenotypic variation, especially biomass or ecophysiological traits, correlating with climatic variables related to precipitation or temperature is less common, but has been reported (Kelly <italic>et al</italic>. <xref rid="b26" ref-type="bibr">2003</xref>; Royer <italic>et al</italic>. <xref rid="b58" ref-type="bibr">2008</xref>; De Kort <italic>et al</italic>. <xref rid="b7" ref-type="bibr">2014</xref>). Overall, these association studies demonstrate the difficulty of linking morphological variation to a single correlating (putatively causative) climate variable. Our multivariate approach allows a landscape-level comparison of population differences, providing evidence of adaptive differentiation at a broad scale (Sork <italic>et al</italic>. <xref rid="b67" ref-type="bibr">2010</xref>; McKown <italic>et al</italic>. <xref rid="b36" ref-type="bibr">2014</xref>).</p><p>The use of <sc>structure</sc> to infer the number of genetic clusters in a collection is an ad hoc application of the software commonly applied in population genetic studies (Pritchard <italic>et al</italic>. <xref rid="b54" ref-type="bibr">2000</xref>). Multiple methods have been proposed to interpret the <sc>structure</sc> results, yet those methods often appear overly conservative (Earl & vonHoldt <xref rid="b13" ref-type="bibr">2012</xref>) or liberal (Falush <italic>et al</italic>. <xref rid="b17" ref-type="bibr">2003</xref>) in assigning the number of genetic clusters. Here, the Earl & vonHoldt (<xref rid="b13" ref-type="bibr">2012</xref>) method indicated <italic>K</italic> = 2, with the Italian samples clustering with those from France and Spain. This pattern varies from those reported in previous studies, where populations from Italy are more similar to the central European trees, and is likely a consequence of the sampling design and limited number of microsatellite data. The Italian trees formed a distinct cluster at <italic>K</italic> = 3 (data not presented). Attempting to identify biologically meaningful differences, we considered the <italic>k</italic> of the highest probability maintaining a small variance, <italic>K</italic> = 5, in which samples clustered according to country of origin, except those from Germany and the Netherlands clustered together. Samples from France were admixed between two genetic clusters. This pattern of admixture and differentiation was more consistent with previous AFLP and microsatellite data (Smulders <italic>et al</italic>. <xref rid="b66" ref-type="bibr">2008</xref>).</p><p>In addition, anthropogenic factors may have contributed to the extant genetic structure of <italic>P. nigra</italic>. Tests of genetic bottlenecks identified three populations that may have recently undergone a population bottleneck. The heterozygosity excess indicated in three populations refers to the levels expected a mutation–drift equilibrium (not Hardy–Weinberg equilibrium), as estimated by the number of alleles in each sample. Human actions may have particularly affected population IT1, sampled along the Ticino River. A previous study reported the depletion of the natural poplar stands in the Ticino River region in northern Italy during the Second World War (Fossati <italic>et al</italic>. <xref rid="b500" ref-type="bibr">2003</xref>), likely contributing to the genetic bottleneck identified from the microsatellite data and demonstrating the potential for management events to affect standing genetic variation in forest trees.</p><p>Understanding how IBD, IBA and IBC individually and jointly affect the genetic structure of a keystone species is critical for conservation and management, especially in context of a changing climate. Numerous models predicting climate changes for the next century have been published, and while results are variable (Blenkinsop & Fowler <xref rid="b2" ref-type="bibr">2007</xref>), some consistent trends have emerged. In Europe, the mean temperature is expected to increase, following a large cline across latitudes, with the greatest increases in the northern areas (Raible <italic>et al</italic>. <xref rid="b55" ref-type="bibr">2006</xref>; Gessler <italic>et al</italic>. <xref rid="b19" ref-type="bibr">2007</xref>). In addition, rates and distribution of precipitation are also expected to change. Models have predicted that summer precipitation will decrease over much of Europe, with levels increasing only in the most northern latitudes (Blenkinsop & Fowler <xref rid="b2" ref-type="bibr">2007</xref>). Drought events are predicted to increase in frequency (Blenkinsop & Fowler <xref rid="b2" ref-type="bibr">2007</xref>; Penuelas <italic>et al</italic>. <xref rid="b49" ref-type="bibr">2007</xref>), especially in southern, Mediterranean areas (Blenkinsop & Fowler <xref rid="b2" ref-type="bibr">2007</xref>). These changes in temperature and precipitation will change the distribution of climate types across Europe. The distribution and abundance of climates analogous to those observed in 1945 (i.e. prewarming) are predicted to decrease in size, increase in fragmentation and generally shift to the northeast, with novel climatic conditions developing (Ohlemuller <italic>et al</italic>. <xref rid="b42" ref-type="bibr">2006</xref>).</p><p>If morphological differentiation strictly tracks differences in environment, then comparing the current distribution of morphotypes and predicted distribution of environments may provide insight for conservation efforts (Sork <italic>et al</italic>. <xref rid="b67" ref-type="bibr">2010</xref>; Kremer <italic>et al</italic>. <xref rid="b28" ref-type="bibr">2012</xref>). However, if the morphological differentiation reflects a combination of adaptive and nonadaptive processes (such as IBC), predicting species response to climate change is further complicated, as the standing genetic variation may not match the most adaptive phenotype for an environment. For example, the <italic>P. nigra</italic> populations from central France (FR4 and FR5) experience a climate more similar to the site in Germany than Spain, but display morphology more similar to the Iberian collections (Fig.<xref ref-type="fig" rid="fig01">1</xref>). If the small-leaf morphotype is adapted to lower or more seasonal precipitation due to their Iberian ancestry (IBC), rather than the current climate, these populations may be ‘pre-adapted’ to higher drought frequency over the next century (Hu & He <xref rid="b23" ref-type="bibr">2006</xref>; Kremer <italic>et al</italic>. <xref rid="b28" ref-type="bibr">2012</xref>). Further, we predict the admixed nature of the populations in France may result in greater plasticity in response to varying environments. An ongoing study of two common garden experiments in contrasting environments (England and Italy) is expected to provide additional insight into the genetic basis of phenotypic differentiation in this important forest tree.</p><p>Together, these patterns of morphological, genetic, geographic and climate differences indicate that IBC due to serial colonization events likely continues to influence the morphological and genetic structure in a forest tree. Genetic structure was significantly correlated with geographic distance but not climatic differences, consistent with models of IBD or isolation by serial colonization. Morphological variation was correlated with both geographic distance and climatic differences. These patterns confirm that multiple evolutionary processes influence the morphological and genetic structure of long-lived species and indicate that the response to climate change may be influenced by historic factors.</p></sec></body><back><ack><p>The authors thank N.R. Street, S. Milner, M. Viger, M. Nelson, M.J. Tallis and M. Goolsby for field, laboratory and ArcGIS assistance. The common garden experiment in Belgium was planted and maintained by M. Steenackers and colleagues. This work was funded by the European Commission 5th Framework Programme for Research project POPYOMICS, the 6th Framework Programme for Research Network of Excellence EVOLTREE and an Overseas Research Student Award Scheme (to JD) and NERC (NER/S/2001/106361). This study does not necessarily reflect the Commission's views and in no way anticipates the Commission's future policy in this area.</p></ack><ref-list><title>References</title><ref id="b1"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Antonovics</surname><given-names>J</given-names></name></person-group><article-title>Evolution in closely adjacent plant populations VI. Manifold effects of gene flow</article-title><source>Heredity</source><year>1968</year><volume>23</volume><fpage>508</fpage><lpage>524</lpage></element-citation></ref><ref id="b2"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Blenkinsop</surname><given-names>S</given-names></name><name><surname>Fowler</surname><given-names>HJ</given-names></name></person-group><article-title>Changes in European drought characteristics projected by the PRUDENCE regional climate models</article-title><source>International Journal of Climatology</source><year>2007</year><volume>27</volume><fpage>1595</fpage><lpage>1610</lpage></element-citation></ref><ref id="b3"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Bock</surname><given-names>DG</given-names></name><name><surname>Andrew</surname><given-names>RL</given-names></name><name><surname>Rieseberg</surname><given-names>L</given-names></name></person-group><article-title>On the adaptive value of cytoplasmic genomes in plants</article-title><source>Molecular Ecology</source><year>2014</year><volume>23</volume><fpage>4899</fpage><lpage>4911</lpage><pub-id pub-id-type="pmid">25223488</pub-id></element-citation></ref><ref id="b4"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Brown</surname><given-names>AHD</given-names></name></person-group><article-title>Isozymes, plant population genetic structure and genetic conservation</article-title><source>Theoretical and Applied Genetics</source><year>1978</year><volume>52</volume><fpage>145</fpage><lpage>157</lpage><pub-id pub-id-type="pmid">24317500</pub-id></element-citation></ref><ref id="b5"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Cavers</surname><given-names>S</given-names></name><name><surname>Navarro</surname><given-names>C</given-names></name><name><surname>Lowe</surname><given-names>AJ</given-names></name></person-group><article-title>Targeting genetic resource conservation in widespread species: a case study of <italic>Cedrela odorata</italic> L</article-title><source>Forest Ecology and Management</source><year>2004</year><volume>197</volume><fpage>285</fpage><lpage>294</lpage></element-citation></ref><ref id="b6"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Cottrell</surname><given-names>JE</given-names></name><name><surname>Krystufek</surname><given-names>V</given-names></name><name><surname>Tabbener</surname><given-names>HE</given-names></name><etal></etal></person-group><article-title>Postglacial migration of <italic>Populus nigra</italic> L.: lessons learnt from chloroplast DNA</article-title><source>Forest Ecology and Management</source><year>2005</year><volume>206</volume><fpage>71</fpage><lpage>90</lpage></element-citation></ref><ref id="b7"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>De Kort</surname><given-names>H</given-names></name><name><surname>Vandepitte</surname><given-names>K</given-names></name><name><surname>Bruun</surname><given-names>HH</given-names></name><etal></etal></person-group><article-title>Landscape genomics and a common garden trial reveal adaptive differentiation to temperature across Europe in the tree species <italic>Alnus glutinosa</italic></article-title><source>Molecular Ecology</source><year>2014</year><volume>23</volume><fpage>4709</fpage><lpage>4721</lpage><pub-id pub-id-type="pmid">24860941</pub-id></element-citation></ref><ref id="b8"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Dennison</surname><given-names>MD</given-names></name><name><surname>Baker</surname><given-names>AJ</given-names></name></person-group><article-title>Morphometric variability in Continental and Atlantic Island Populations of Chaffinches (<italic>Fringilla coelebs</italic></article-title><source>Evolution</source><year>1991</year><volume>45</volume><fpage>29</fpage><lpage>39</lpage></element-citation></ref><ref id="b9"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>DeWoody</surname><given-names>J</given-names></name><name><surname>Nason</surname><given-names>JD</given-names></name><name><surname>Hipkins</surname><given-names>VD</given-names></name></person-group><article-title>Mitigating scoring errors in microsatellite data from wild populations</article-title><source>Molecular Ecology Notes</source><year>2006</year><volume>6</volume><fpage>951</fpage><lpage>957</lpage></element-citation></ref><ref id="b10"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Dudley</surname><given-names>SA</given-names></name></person-group><article-title>Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses</article-title><source>Evolution</source><year>1996a</year><volume>50</volume><fpage>92</fpage><lpage>102</lpage></element-citation></ref><ref id="b11"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Dudley</surname><given-names>SA</given-names></name></person-group><article-title>The response to differing selection on plant physiological traits: evidence for local adaptation</article-title><source>Evolution</source><year>1996b</year><volume>50</volume><fpage>103</fpage><lpage>110</lpage></element-citation></ref><ref id="b12"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Duminil</surname><given-names>J</given-names></name><name><surname>Fineschi</surname><given-names>S</given-names></name><name><surname>Hampe</surname><given-names>A</given-names></name><etal></etal></person-group><article-title>Can population genetic structure be predicted from life-history traits?</article-title><source>American Naturalist</source><year>2007</year><volume>169</volume><fpage>662</fpage><lpage>672</lpage></element-citation></ref><ref id="b13"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Earl</surname><given-names>DA</given-names></name><name><surname>vonHoldt</surname><given-names>BM</given-names></name></person-group><article-title>STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method</article-title><source>Conservation Genetics Resources</source><year>2012</year><volume>4</volume><fpage>359</fpage><lpage>361</lpage></element-citation></ref><ref id="b14"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Eckert</surname><given-names>CG</given-names></name><name><surname>Manicacci</surname><given-names>D</given-names></name><name><surname>Barrett</surname><given-names>SCH</given-names></name></person-group><article-title>Genetic drift and founder effect in native versus introduced populations of an invading plant, <italic>Lythrum salicaria</italic> (Lythraceae)</article-title><source>Evolution</source><year>1996</year><volume>50</volume><fpage>1512</fpage><lpage>1519</lpage></element-citation></ref><ref id="b15"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Evanno</surname><given-names>G</given-names></name><name><surname>Regnaut</surname><given-names>S</given-names></name><name><surname>Goudet</surname><given-names>J</given-names></name></person-group><article-title>Detecting the number of clusters of individuals using the software structure: a simulation study</article-title><source>Molecular Ecology</source><year>2005</year><volume>14</volume><fpage>2611</fpage><lpage>2620</lpage><pub-id pub-id-type="pmid">15969739</pub-id></element-citation></ref><ref id="b16"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Fabbrini</surname><given-names>F</given-names></name><name><surname>Gaudet</surname><given-names>M</given-names></name><name><surname>Bastien</surname><given-names>C</given-names></name><etal></etal></person-group><article-title>Phenotypic plasticity, QTL mapping and genomic characterization of bud set in black poplar</article-title><source>BMC Plant Biology</source><year>2012</year><volume>12</volume><fpage>47</fpage><pub-id pub-id-type="pmid">22471289</pub-id></element-citation></ref><ref id="b17"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Falush</surname><given-names>D</given-names></name><name><surname>Stephens</surname><given-names>M</given-names></name><name><surname>Pritchard</surname><given-names>JK</given-names></name></person-group><article-title>Inference of population structure: extensions to linked loci and correlated allele frequencies</article-title><source>Genetics</source><year>2003</year><volume>164</volume><fpage>1567</fpage><lpage>1587</lpage><pub-id pub-id-type="pmid">12930761</pub-id></element-citation></ref><ref id="b500"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Fossati</surname><given-names>T</given-names></name><name><surname>Grassi</surname><given-names>F</given-names></name><name><surname>Sala</surname><given-names>F</given-names></name><name><surname>Castiglione</surname><given-names>S</given-names></name></person-group><article-title>Molecular analysis of natural populations of Populus nigra L. intermingled with cultivated hybrids</article-title><source>Molecular Ecology</source><year>2003</year><volume>12</volume><fpage>2033</fpage><lpage>2043</lpage><pub-id pub-id-type="pmid">12859627</pub-id></element-citation></ref><ref id="b18"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Gailing</surname><given-names>O</given-names></name><name><surname>Lind</surname><given-names>J</given-names></name><name><surname>Lilleskov</surname><given-names>E</given-names></name></person-group><article-title>Leaf morphological and genetic differentiation between <italic>Quercus rubra</italic> L. and <italic>Q. ellipsoidalis</italic> E.J. Hill populations in contrasting environments</article-title><source>Plant Systematics and Evolution</source><year>2012</year><volume>298</volume><fpage>1533</fpage><lpage>1545</lpage></element-citation></ref><ref id="b19"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Gessler</surname><given-names>A</given-names></name><name><surname>Keitel</surname><given-names>C</given-names></name><name><surname>Kreuzwieser</surname><given-names>J</given-names></name><etal></etal></person-group><article-title>Potential risks for European beech (<italic>Fagus sylvatica</italic> L.) in a changing climate</article-title><source>Trees-Structure and Function</source><year>2007</year><volume>21</volume><fpage>1</fpage><lpage>11</lpage></element-citation></ref><ref id="b20"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hall</surname><given-names>D</given-names></name><name><surname>Luquez</surname><given-names>V</given-names></name><name><surname>Garcia</surname><given-names>VM</given-names></name><etal></etal></person-group><article-title>Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (<italic>Populus tremula</italic>, L.): a comparison of neutral markers, candidate genes and phenotypic traits</article-title><source>Evolution</source><year>2007</year><volume>61</volume><fpage>2849</fpage><lpage>2860</lpage><pub-id pub-id-type="pmid">17908247</pub-id></element-citation></ref><ref id="b21"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hamrick</surname><given-names>JL</given-names></name><name><surname>Godt</surname><given-names>MJW</given-names></name></person-group><article-title>Effects of life history traits on genetic diversity in plant species</article-title><source>Philosophical Transactions of the Royal Society B-Biological Sciences</source><year>1996</year><volume>351</volume><fpage>1291</fpage><lpage>1298</lpage></element-citation></ref><ref id="b22"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hijmans</surname><given-names>RJ</given-names></name><name><surname>Cameron</surname><given-names>SE</given-names></name><name><surname>Parra</surname><given-names>JL</given-names></name><name><surname>Jones</surname><given-names>PG</given-names></name><name><surname>Jarvis</surname><given-names>A</given-names></name></person-group><article-title>Very high resolution interpolated climate surfaces for global land areas</article-title><source>International Journal of Climatology</source><year>2005</year><volume>25</volume><fpage>1965</fpage><lpage>1978</lpage></element-citation></ref><ref id="b23"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hu</surname><given-names>X-S</given-names></name><name><surname>He</surname><given-names>F</given-names></name></person-group><article-title>Seed and pollen flow in expanding a species' range</article-title><source>Journal of Theoretical Biology</source><year>2006</year><volume>240</volume><fpage>662</fpage><lpage>672</lpage><pub-id pub-id-type="pmid">16364367</pub-id></element-citation></ref><ref id="b24"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Jensen</surname><given-names>JL</given-names></name><name><surname>Bohonak</surname><given-names>AJ</given-names></name><name><surname>Kelley</surname><given-names>ST</given-names></name></person-group><article-title>Isolation by distance, web service</article-title><source>BMC Genetics</source><year>2005</year><volume>6</volume><fpage>13</fpage><pub-id pub-id-type="pmid">15760479</pub-id></element-citation></ref><ref id="b25"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kawecki</surname><given-names>TJ</given-names></name><name><surname>Evert</surname><given-names>D</given-names></name></person-group><article-title>Conceptual issues in local adaptation</article-title><source>Ecology Letters</source><year>2004</year><volume>7</volume><fpage>1225</fpage><lpage>1241</lpage></element-citation></ref><ref id="b26"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kelly</surname><given-names>CK</given-names></name><name><surname>Chase</surname><given-names>MW</given-names></name><name><surname>De Bruijn</surname><given-names>A</given-names></name><name><surname>Fay</surname><given-names>MF</given-names></name><name><surname>Woodward</surname><given-names>FI</given-names></name></person-group><article-title>Temperature-based population segregation in birch</article-title><source>Ecology Letters</source><year>2003</year><volume>6</volume><fpage>87</fpage><lpage>89</lpage></element-citation></ref><ref id="b27"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kremer</surname><given-names>A</given-names></name><name><surname>Kleinschmit</surname><given-names>J</given-names></name><name><surname>Cottrell</surname><given-names>J</given-names></name><etal></etal></person-group><article-title>Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks?</article-title><source>Forest Ecology and Management</source><year>2002</year><volume>156</volume><fpage>75</fpage><lpage>87</lpage></element-citation></ref><ref id="b28"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kremer</surname><given-names>A</given-names></name><name><surname>Ronce</surname><given-names>O</given-names></name><name><surname>Robledo-Arnuncio</surname><given-names>JJ</given-names></name><etal></etal></person-group><article-title>Long-distance gene flow and adaptation of forest trees to rapid climate change</article-title><source>Ecology Letters</source><year>2012</year><volume>15</volume><fpage>378</fpage><lpage>392</lpage><pub-id pub-id-type="pmid">22372546</pub-id></element-citation></ref><ref id="b29"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>LeCorre</surname><given-names>V</given-names></name><name><surname>Kremer</surname><given-names>A</given-names></name></person-group><article-title>Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection</article-title><source>Genetics</source><year>2003</year><volume>164</volume><fpage>1205</fpage><lpage>1219</lpage><pub-id pub-id-type="pmid">12871925</pub-id></element-citation></ref><ref id="b30"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Leinonen</surname><given-names>T</given-names></name><name><surname>McCairns</surname><given-names>RJS</given-names></name><name><surname>O'Hara</surname><given-names>RB</given-names></name><name><surname>Merila</surname><given-names>J</given-names></name></person-group><article-title><italic>Q</italic>st-<italic>F</italic>st comparisons: evolutionary and ecological insights from genomic heterogeneity</article-title><source>Nature Reviews Genetics</source><year>2013</year><volume>14</volume><fpage>179</fpage><lpage>190</lpage></element-citation></ref><ref id="b31"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Loveless</surname><given-names>MD</given-names></name><name><surname>Hamrick</surname><given-names>JL</given-names></name></person-group><article-title>Ecological determinants of genetic structure in plant populations</article-title><source>Annual Review of Ecology and Systematics</source><year>1984</year><volume>15</volume><fpage>65</fpage><lpage>95</lpage></element-citation></ref><ref id="b32"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Luikart</surname><given-names>G</given-names></name><name><surname>Cornuet</surname><given-names>J-M</given-names></name></person-group><article-title>Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data</article-title><source>Conservation Biology</source><year>1998</year><volume>12</volume><fpage>228</fpage><lpage>237</lpage></element-citation></ref><ref id="b33"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Luikart</surname><given-names>G</given-names></name><name><surname>Sherwin</surname><given-names>WB</given-names></name><name><surname>Steele</surname><given-names>BM</given-names></name><name><surname>Allendorf</surname><given-names>FW</given-names></name></person-group><article-title>Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change</article-title><source>Molecular Ecology</source><year>1998</year><volume>7</volume><fpage>963</fpage><lpage>974</lpage><pub-id pub-id-type="pmid">9711862</pub-id></element-citation></ref><ref id="b34"><element-citation publication-type="book"><person-group person-group-type="author"><name><surname>Manly</surname><given-names>BFJ</given-names></name></person-group><source>Randomization, Bootstrap and Monte Carlo Methods in Biology</source><year>1997</year><edition>2nd edn</edition><publisher-loc>London</publisher-loc><publisher-name>Chapman & Hall</publisher-name></element-citation></ref><ref id="b35"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>McKay</surname><given-names>JK</given-names></name><name><surname>Latta</surname><given-names>RG</given-names></name></person-group><article-title>Adaptive population divergence: markers, QTL and traits</article-title><source>Trends in Ecology & Evolution</source><year>2002</year><volume>17</volume><fpage>285</fpage><lpage>291</lpage></element-citation></ref><ref id="b36"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>McKown</surname><given-names>AD</given-names></name><name><surname>Guy</surname><given-names>RD</given-names></name><name><surname>Klapste</surname><given-names>J</given-names></name><etal></etal></person-group><article-title>Geographical and environmental gradients shape phenotypic trait variation and genetic structure in <italic>Populus trichocarpa</italic></article-title><source>New Phytologist</source><year>2014</year><volume>201</volume><fpage>1263</fpage><lpage>1276</lpage><pub-id pub-id-type="pmid">24491114</pub-id></element-citation></ref><ref id="b37"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Merila</surname><given-names>J</given-names></name><name><surname>Crnokrak</surname><given-names>P</given-names></name></person-group><article-title>Comparison of genetic differentiation at marker loci and quantitative traits</article-title><source>Journal of Evolutionary Biology</source><year>2001</year><volume>14</volume><fpage>892</fpage><lpage>903</lpage></element-citation></ref><ref id="b38"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mitton</surname><given-names>JB</given-names></name><name><surname>Duran</surname><given-names>KL</given-names></name></person-group><article-title>Genetic variation in piñon pine, <italic>Pinus edulis</italic>, associated with summer precipitation</article-title><source>Molecular Ecology</source><year>2004</year><volume>13</volume><fpage>1259</fpage><lpage>1264</lpage><pub-id pub-id-type="pmid">15078461</pub-id></element-citation></ref><ref id="b39"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Moya-Larano</surname><given-names>J</given-names></name><name><surname>Corcobado</surname><given-names>G</given-names></name></person-group><article-title>Plotting partial correlation and regression in ecological studies</article-title><source>Web Ecology</source><year>2008</year><volume>8</volume><fpage>35</fpage><lpage>46</lpage></element-citation></ref><ref id="b40"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Nason</surname><given-names>JD</given-names></name><name><surname>Hamrick</surname><given-names>JL</given-names></name><name><surname>Fleming</surname><given-names>TH</given-names></name></person-group><article-title>Historical vicariance and postglacial colonization effects on the evolution of genetic structure in <italic>Lophocereus</italic>, a Sonoran desert columnar cactus</article-title><source>Evolution</source><year>2002</year><volume>56</volume><fpage>2214</fpage><lpage>2226</lpage><pub-id pub-id-type="pmid">12487352</pub-id></element-citation></ref><ref id="b41"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Nosil</surname><given-names>P</given-names></name><name><surname>Funk</surname><given-names>DJ</given-names></name><name><surname>Ortiz-Barrientos</surname><given-names>D</given-names></name></person-group><article-title>Divergent selection and heterogeneous genomic divergence</article-title><source>Molecular Ecology</source><year>2009</year><volume>18</volume><fpage>375</fpage><lpage>402</lpage><pub-id pub-id-type="pmid">19143936</pub-id></element-citation></ref><ref id="b42"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Ohlemuller</surname><given-names>R</given-names></name><name><surname>Gritti</surname><given-names>ES</given-names></name><name><surname>Sykes</surname><given-names>MT</given-names></name><name><surname>Thomas</surname><given-names>CD</given-names></name></person-group><article-title>Towards European climate risk surfaces: the extent and distribution of analogous and non-analogous climates 1931-2100</article-title><source>Global Ecology and Biogeography</source><year>2006</year><volume>15</volume><fpage>395</fpage><lpage>405</lpage></element-citation></ref><ref id="b43"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>van Oosterhout</surname><given-names>C</given-names></name><name><surname>Hutchinson</surname><given-names>WF</given-names></name><name><surname>Willis</surname><given-names>DPM</given-names></name><name><surname>Shipley</surname><given-names>P</given-names></name></person-group><article-title>MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data</article-title><source>Molecular Ecology Notes</source><year>2004</year><volume>4</volume><fpage>535</fpage><lpage>538</lpage></element-citation></ref><ref id="b44"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Orsini</surname><given-names>L</given-names></name><name><surname>Corander</surname><given-names>J</given-names></name><name><surname>Alasentie</surname><given-names>A</given-names></name><name><surname>Hanski</surname><given-names>I</given-names></name></person-group><article-title>Genetic spatial structure in a butterfly metapopulation correlates better with past than present demographic structure</article-title><source>Molecular Ecology</source><year>2008</year><volume>17</volume><fpage>2629</fpage><lpage>2642</lpage><pub-id pub-id-type="pmid">18466229</pub-id></element-citation></ref><ref id="b45"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Orsini</surname><given-names>L</given-names></name><name><surname>Vanoverbeke</surname><given-names>J</given-names></name><name><surname>Swillen</surname><given-names>I</given-names></name><name><surname>Mergeay</surname><given-names>J</given-names></name><name><surname>De Meester</surname><given-names>L</given-names></name></person-group><article-title>Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization</article-title><source>Molecular Ecology</source><year>2013</year><volume>22</volume><fpage>5983</fpage><lpage>5999</lpage><pub-id pub-id-type="pmid">24128305</pub-id></element-citation></ref><ref id="b46"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Palme</surname><given-names>AE</given-names></name><name><surname>Su</surname><given-names>Q</given-names></name><name><surname>Rautenberg</surname><given-names>A</given-names></name><name><surname>Manni</surname><given-names>F</given-names></name><name><surname>Lascoux</surname><given-names>M</given-names></name></person-group><article-title>Postglacial recolonization and cpDNA variation of silver birch, <italic>Betula pendula</italic></article-title><source>Molecular Ecology</source><year>2003</year><volume>12</volume><fpage>201</fpage><lpage>212</lpage><pub-id pub-id-type="pmid">12492888</pub-id></element-citation></ref><ref id="b47"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Peakall</surname><given-names>R</given-names></name><name><surname>Smouse</surname><given-names>PE</given-names></name></person-group><article-title>GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research</article-title><source>Molecular Ecology Notes</source><year>2006</year><volume>6</volume><fpage>288</fpage><lpage>295</lpage></element-citation></ref><ref id="b48"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Peakall</surname><given-names>R</given-names></name><name><surname>Smouse</surname><given-names>PE</given-names></name><name><surname>Huff</surname><given-names>DR</given-names></name></person-group><article-title>Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss <italic>Buchloë dactyloides</italic></article-title><source>Molecular Ecology</source><year>1995</year><volume>4</volume><fpage>135</fpage><lpage>147</lpage></element-citation></ref><ref id="b49"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Penuelas</surname><given-names>J</given-names></name><name><surname>Prieto</surname><given-names>P</given-names></name><name><surname>Beier</surname><given-names>C</given-names></name><etal></etal></person-group><article-title>Response of plant species richness and primary productivity in shrublands along a north-south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003</article-title><source>Global Change Biology</source><year>2007</year><volume>13</volume><fpage>2563</fpage><lpage>2581</lpage></element-citation></ref><ref id="b50"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Petit</surname><given-names>RJ</given-names></name><name><surname>Csaikl</surname><given-names>UM</given-names></name><name><surname>Bordacs</surname><given-names>S</given-names></name><etal></etal></person-group><article-title>Chloroplast DNA variation in European white oaks – Phylogeography and patterns of diversity based on data from over 2600 populations</article-title><source>Forest Ecology and Management</source><year>2002</year><volume>156</volume><fpage>5</fpage><lpage>26</lpage></element-citation></ref><ref id="b51"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Petit</surname><given-names>RJ</given-names></name><name><surname>Aguinagalde</surname><given-names>I</given-names></name><name><surname>de Beaulieu</surname><given-names>JL</given-names></name><etal></etal></person-group><article-title>Glacial refugia: hotspots but not melting pots of genetic diversity</article-title><source>Science</source><year>2003</year><volume>300</volume><fpage>1563</fpage><lpage>1565</lpage><pub-id pub-id-type="pmid">12791991</pub-id></element-citation></ref><ref id="b52"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Picotte</surname><given-names>J</given-names></name><name><surname>Rosenthal</surname><given-names>D</given-names></name><name><surname>Rhode</surname><given-names>J</given-names></name><name><surname>Cruzan</surname><given-names>M</given-names></name></person-group><article-title>Plastic responses to temporal variation in moisture availability: consequences for water use efficiency and plant performance</article-title><source>Oecologia</source><year>2007</year><volume>153</volume><fpage>821</fpage><lpage>832</lpage><pub-id pub-id-type="pmid">17636336</pub-id></element-citation></ref><ref id="b53"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Poorter</surname><given-names>H</given-names></name><name><surname>Niinemets</surname><given-names>Ü</given-names></name><name><surname>Poorter</surname><given-names>L</given-names></name><name><surname>Wright</surname><given-names>IJ</given-names></name><name><surname>Villar</surname><given-names>R</given-names></name></person-group><article-title>Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis</article-title><source>New Phytologist</source><year>2009</year><volume>182</volume><fpage>565</fpage><lpage>588</lpage><pub-id pub-id-type="pmid">19434804</pub-id></element-citation></ref><ref id="b54"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Pritchard</surname><given-names>JK</given-names></name><name><surname>Stephens</surname><given-names>M</given-names></name><name><surname>Donnelley</surname><given-names>P</given-names></name></person-group><article-title>Inference of population structure using multilocus genotype data</article-title><source>Genetics</source><year>2000</year><volume>155</volume><fpage>945</fpage><lpage>959</lpage><pub-id pub-id-type="pmid">10835412</pub-id></element-citation></ref><ref id="b55"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Raible</surname><given-names>CC</given-names></name><name><surname>Casty</surname><given-names>C</given-names></name><name><surname>Luterbacher</surname><given-names>J</given-names></name><etal></etal></person-group><article-title>Climate variability-observations, reconstructions, and model simulations for the Atlantic-European and Alpine region from 1500-2100 AD</article-title><source>Climatic Change</source><year>2006</year><volume>79</volume><fpage>9</fpage><lpage>29</lpage></element-citation></ref><ref id="b56"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Rohde</surname><given-names>A</given-names></name><name><surname>Storme</surname><given-names>V</given-names></name><name><surname>Jorge</surname><given-names>V</given-names></name><etal></etal></person-group><article-title>Bud set in poplar – genetic dissection of a complex trait in natural and hybrid populations</article-title><source>New Phytologist</source><year>2011</year><volume>189</volume><fpage>106</fpage><lpage>121</lpage><pub-id pub-id-type="pmid">21039557</pub-id></element-citation></ref><ref id="b57"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Rousset</surname><given-names>F</given-names></name></person-group><article-title>Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance</article-title><source>Genetics</source><year>1997</year><volume>145</volume><fpage>1219</fpage><lpage>1228</lpage><pub-id pub-id-type="pmid">9093870</pub-id></element-citation></ref><ref id="b58"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Royer</surname><given-names>DL</given-names></name><name><surname>McElwain</surname><given-names>JC</given-names></name><name><surname>Adams</surname><given-names>JM</given-names></name><name><surname>Wilf</surname><given-names>P</given-names></name></person-group><article-title>Sensitivity of leaf size and shape to climate within <italic>Acer rubrum</italic> and <italic>Quercus kelloggii</italic></article-title><source>New Phytologist</source><year>2008</year><volume>179</volume><fpage>808</fpage><lpage>817</lpage><pub-id pub-id-type="pmid">18507771</pub-id></element-citation></ref><ref id="b59"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Salmela</surname><given-names>MJ</given-names></name></person-group><article-title>Rethinking local adaptaiton: mind the environment!</article-title><source>Forest Ecology and Management</source><year>2014</year><volume>312</volume><fpage>271</fpage><lpage>281</lpage></element-citation></ref><ref id="b60"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Savolainen</surname><given-names>O</given-names></name><name><surname>Pyhajarvi</surname><given-names>T</given-names></name></person-group><article-title>Genomic diversity in forest trees</article-title><source>Current Opinion in Plant Biology</source><year>2007</year><volume>10</volume><fpage>162</fpage><lpage>167</lpage><pub-id pub-id-type="pmid">17292660</pub-id></element-citation></ref><ref id="b61"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Savolainen</surname><given-names>O</given-names></name><name><surname>Lascoux</surname><given-names>M</given-names></name><name><surname>Merlia</surname><given-names>J</given-names></name></person-group><article-title>Ecological genomics of local adaptation</article-title><source>Nature Reviews Genetics</source><year>2013</year><volume>14</volume><fpage>807</fpage><lpage>820</lpage></element-citation></ref><ref id="b62"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Slatkin</surname><given-names>M</given-names></name></person-group><article-title>Isolation by distance in equilibrium and non-equilibrium populations</article-title><source>Evolution</source><year>1993</year><volume>47</volume><fpage>264</fpage><lpage>279</lpage></element-citation></ref><ref id="b63"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Smouse</surname><given-names>PE</given-names></name><name><surname>Peakall</surname><given-names>R</given-names></name></person-group><article-title>Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure</article-title><source>Heredity</source><year>1999</year><volume>82</volume><fpage>561</fpage><lpage>573</lpage><pub-id pub-id-type="pmid">10383677</pub-id></element-citation></ref><ref id="b64"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Smouse</surname><given-names>PE</given-names></name><name><surname>Long</surname><given-names>JC</given-names></name><name><surname>Sokal</surname><given-names>RR</given-names></name></person-group><article-title>Multiple regression and correlation extensions of the Mantel test of matrix correspondence</article-title><source>Systematic Zoology</source><year>1986</year><volume>35</volume><fpage>627</fpage><lpage>632</lpage></element-citation></ref><ref id="b65"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Smulders</surname><given-names>MJM</given-names></name><name><surname>van der Schoot</surname><given-names>J</given-names></name><name><surname>Arens</surname><given-names>P</given-names></name><name><surname>Vosman</surname><given-names>B</given-names></name></person-group><article-title>Trinucleotide repeat microsatellite markers for black poplar (<italic>Populus nigra</italic> L.)</article-title><source>Molecular Ecology Notes</source><year>2001</year><volume>1</volume><fpage>188</fpage><lpage>190</lpage></element-citation></ref><ref id="b66"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Smulders</surname><given-names>MJM</given-names></name><name><surname>Cottrell</surname><given-names>JE</given-names></name><name><surname>Lefevre</surname><given-names>F</given-names></name><etal></etal></person-group><article-title>Structure of the genetic diversity in black poplar (<italic>Populus nigra</italic> L.) populations across European river systems: consequences for conservation and restoration</article-title><source>Forest Ecology and Management</source><year>2008</year><volume>255</volume><fpage>1388</fpage><lpage>1399</lpage></element-citation></ref><ref id="b67"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Sork</surname><given-names>VL</given-names></name><name><surname>Davis</surname><given-names>FW</given-names></name><name><surname>Westfall</surname><given-names>R</given-names></name><etal></etal></person-group><article-title>Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Née) in the face of climate change</article-title><source>Molecular Ecology</source><year>2010</year><volume>19</volume><fpage>3806</fpage><lpage>3823</lpage><pub-id pub-id-type="pmid">20723054</pub-id></element-citation></ref><ref id="b68"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Spurgin</surname><given-names>LG</given-names></name><name><surname>Illera</surname><given-names>JC</given-names></name><name><surname>Jorgensen</surname><given-names>TH</given-names></name><name><surname>Dawson</surname><given-names>DA</given-names></name><name><surname>Richardson</surname><given-names>DS</given-names></name></person-group><article-title>Genetic and phenotypic divergence in an island bird: isolation by distance, by colonization, or by adaptation?</article-title><source>Molecular Ecology</source><year>2014</year><volume>23</volume><fpage>1028</fpage><lpage>1039</lpage><pub-id pub-id-type="pmid">24447303</pub-id></element-citation></ref><ref id="b69"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Steane</surname><given-names>D</given-names></name><name><surname>Conod</surname><given-names>N</given-names></name><name><surname>Jones</surname><given-names>R</given-names></name><name><surname>Vaillancourt</surname><given-names>R</given-names></name><name><surname>Potts</surname><given-names>B</given-names></name></person-group><article-title>A comparative analysis of population structure of a forest tree, <italic>Eucalyptus globulus</italic> (Myrtaceae), using microsatellite markers and quantitative traits</article-title><source>Tree Genetics & Genomes</source><year>2006</year><volume>2</volume><fpage>30</fpage><lpage>38</lpage></element-citation></ref><ref id="b70"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Turesson</surname><given-names>G</given-names></name></person-group><article-title>The genotypical response of the plant species to the habitat</article-title><source>Hereditas</source><year>1922</year><volume>3</volume><fpage>211</fpage><lpage>350</lpage></element-citation></ref><ref id="b71"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Tzedakis</surname><given-names>PC</given-names></name><name><surname>Emerson</surname><given-names>BC</given-names></name><name><surname>Hewitt</surname><given-names>GM</given-names></name></person-group><article-title>Cryptic or mystic? Glacial tree refugia in northern Europe</article-title><source>Trends in Ecology & Evolution</source><year>2013</year><volume>28</volume><fpage>696</fpage><lpage>704</lpage><pub-id pub-id-type="pmid">24091207</pub-id></element-citation></ref><ref id="b72"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Vendramin</surname><given-names>GG</given-names></name><name><surname>Anzidei</surname><given-names>M</given-names></name><name><surname>Madaghiele</surname><given-names>A</given-names></name><name><surname>Sperisen</surname><given-names>C</given-names></name><name><surname>Bucci</surname><given-names>G</given-names></name></person-group><article-title>Chloroplast microsatellite analysis reveals the presence of population subdivision in Norway spruce (<italic>Picea abies</italic> K.)</article-title><source>Genome</source><year>2000</year><volume>43</volume><fpage>68</fpage><lpage>78</lpage><pub-id pub-id-type="pmid">10701115</pub-id></element-citation></ref><ref id="b73"><element-citation publication-type="other"><person-group person-group-type="author"><name><surname>Viger</surname><given-names>M</given-names></name></person-group><year>2011</year><fpage>258</fpage><comment><italic>Physiology, genetics and genomics of drought adaptation in</italic> Populus. Doctoral Thesis, University of Southampton, Centre for Biological Sciences, Southampton, UK</comment></element-citation></ref><ref id="b74"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Westoby</surname><given-names>M</given-names></name><name><surname>Wright</surname><given-names>IJ</given-names></name></person-group><article-title>Land-plant ecology on the basis of functional traits</article-title><source>Trends in Ecology & Evolution</source><year>2006</year><volume>21</volume><fpage>261</fpage><lpage>268</lpage><pub-id pub-id-type="pmid">16697912</pub-id></element-citation></ref><ref id="b75"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Wright</surname><given-names>S</given-names></name></person-group><article-title>Evolution in Mendelian populations</article-title><source>Genetics</source><year>1931</year><volume>16</volume><fpage>97</fpage><lpage>159</lpage><pub-id pub-id-type="pmid">17246615</pub-id></element-citation></ref><ref id="b76"><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Yang</surname><given-names>X-D</given-names></name><name><surname>Yan</surname><given-names>E-R</given-names></name><name><surname>Chang</surname><given-names>SX</given-names></name><etal></etal></person-group><article-title>Twig-leaf size relationships in woody plants vary intraspecifically along a soil moisture gradient</article-title><source>Acta Oecologica</source><year>2014</year><volume>60</volume><fpage>17</fpage><lpage>25</lpage></element-citation></ref></ref-list><sec><title>Data accessibility</title><p>Morphological measures, microsatellite data and climate details are available in the Dryad Digital Repository under doi: 10.5061/dryad.kq0n5.</p></sec><sec sec-type="supplementary-material"><title>Supporting information</title><p>Additional supporting information may be found in the online version of this article.</p><supplementary-material content-type="local-data" id="SD1"><caption><p><bold>Fig. S1</bold> Results of the <sc>structure</sc> and <sc>structure harvester</sc> analyses of microsatellite data.</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="mec0024-2641-sd1.pdf" xlink:type="simple" id="d36e4872" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="SD2"><caption><p><bold>Methods S1</bold> Details of microsatellite analyses and morphological data collection, with associated references.</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="mec0024-2641-sd2.pdf" xlink:type="simple" id="d36e4879" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="SD3"><caption><p><bold>Tables S1–S5</bold> Correlation among climatic variables; Per-locus <italic>F</italic><sub>ST</sub> values; Phenotypic variation measured at 12 traits in trees from 13 populations grown in a common garden study; Correlation among population means for 12 morphological traits.</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="mec0024-2641-sd3.pdf" xlink:type="simple" id="d36e4891" position="anchor"></media></supplementary-material></sec></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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