73Climatedrivenreductionofgeneticvariationi

PRIMARYRESEARCHARTICLEClimate‐drivenreductionofgeneticvariationinplantphenologyalterssoilcommunitiesandnutrientpoolsIanM.Ware1|MichaelE.VanNuland2|JenniferA.Schweitzer1|ZaminYang3|ChristopherW.Schadt3,4|LindsayC.Sidak‐Loftis5|NathanE.Stone5|JosephD.Busch5|DavidM.Wagner5|JosephK.Bailey11DepartmentofEcologyandEvolutionaryBiology,UniversityofTennessee,Knoxville,Tennessee2DeparmentofBiology,StanfordUniversity,Stanford,California3BioscienceDivision,OakRidgeNationalLaboratory,OakRidge,Tennessee4DepartmentofMicrobiology,UniversityofTennessee,Knoxville,Tennessee5PathogenandMicrobiomeInstitute,NorthernArizonaUniversity,Flagstaff,ArizonaCorrespondenceIanM.Ware,UniversityofTennessee,Knoxville,TN.Email:[e-mail]versityofTennessee,Knoxville;GenomicScienceProgram,USDept.ofEnergy,aspartofthePlantMicrobeInterfacesScientificFocusArea;CowdenEndowmentatNorthernArizonaUniversityAbstractWeexaminedthehypothesisthatclimate‐drivenevolutionofplanttraitswillinflu-enceassociatedsoilmicrobiomesandecosystemfunctionacrossthelandscape.Usingafoundationtreespecies,Populusangustifolia,observationalandcommongar-denapproaches,andabasepopulationgeneticcollectionthatspans17riversys-temsinthewesternUnitedStates,fromAZtoMT,weshowthat(a)asmeanannualtemperature(MAT)increases,geneticandphenotypicvariationforbudbreakphenologydecline;(b)soilmicrobiomes,soilnitrogen(N),andsoilcarbon(C)varyinresponsetoMATandconditioningbytrees;and(c)withlossesofgeneticvariationduetowarming,population‐levelregulationofcommunityandecosystemfunctionsstrengthen.Theseresultsdemonstratearelationshipbetweenthepotentialevolu-tionaryresponseofpopulationsandsubsequentshiftsinecosystemfunctionalongalargetemperaturegradient.KEYWORDSclimate,ecosystemdynamics,geneticdivergence,intraspecificvariation,phenology,Populus1|INTRODUCTIONUnderstandinghowclimatechangemaydriveevolutioninplanttraitsthatleadtoshiftsincommunitystructureandecosystemfunctionremainsafrontierinmodernecologyandwillbecomeincreasinglyimportantasglobalenvironmentscontinuetowarm(Baileyetal.,2014;Gilman,Urban,Tewksbury,Gilchrist,&Holt,2010;Lavergne,Mouquet,Thuiller,&Ronce,2010;Woolbright,Whitham,Gehring,Allan,&Bailey,2014).Thelackoflong‐term,well‐replicateddataatspatialscalesrelevanttoprojectedclimatechangescenariosmakeitdifficulttoproducecomprehensivestudiesandpredictionsaboutinherentlylinkedecologicalandevolutionaryresponsesacrossmulti-plelevelsoforganization(i.e.,fromgenestoecosystems).However,existingplantpopulationsthataretheresultofpastclimate‐drivenrangeshiftscanbeusefulforunderstandingtheconsequencesofclimatechangeeventsbecausetheypersistinsuitableextanthabitatpatchesthatarepotentiallyneartheedgeoftheirclimatethreshold.Asaresult,theyareoftenlocallyadaptedtotheenvironmentalcondi-tionsinwhichtheypersistbecauseofnaturalselection,geneticdrift,andminimalgeneflowamongpopulations(reviewedinRehm,Olivas,Stroud,&Feeley,2015;Woolbrightetal.,2014).MaladaptationcanoccurduetocontinualgeneflowfrommorecentralpopulationsorAlleeeffectsifpopulationsizereachesacriticalminimumthreshold(Angert&Schemske2007;Kirkpatrick&Barton,1997;Sexton,McIn-tyre,Angert,&Rice,2009).However,thereisampleevidencedocu-mentingecologicalandevolutionarychangesinnaturalsystemsrespondingtomodernclimatechangescenarios(Lustenhouwer,Wilschut,Williams,Putten,&Levine,2017;Parmesan,2006;Walther,2010).Thus,investigatingpatternsofintraspecificgeneticvariationReceived:2May2018|Accepted:7December2018DOI:10.1111/gcb.14553GlobChangeBiol.2019;1–15.wileyonlinelibrary.com/journal/gcb©2019JohnWiley&SonsLtd|1acrosspopulationscouldproveimportantforpredictingadaptiveresponsestofuturechangesinclimate.Plantphenologicaltraitsshowstronggeneticdifferentiationalongnaturalclimaticgradientsassoci-atedwithlatitudinalandelevationalclines(Kooyers,Greenlee,Coloic-chio,Oh,&Blackman,2015;Peterson,Doak,&Morris,2017;Rohdeetal.,2011;Wadgymar,Daws,&Anderson,2017),oftenresultinginlocallyadaptedecotypes(Aitken,Yeaman,Holliday,Wang,&Curtis‐McLane,2008andreferencestherein).However,abioticandbioticsoilcharacteristicsaregainingappreciationasecologicallyimportantfactorsinpredictingvariationinavarietyofphenologytraits.Forexample,differencesinsoilfertilizationtreatments,soilchemistry,andsoilmicrobialcommunitieshavebeendirectlylinkedtochangesinphenologicaltraitvariation(Arend,Gessler,&Schaub,2016;Sig-urdsson,2001;Wagneretal.,2014).Further,springemergenceoffoliartissue(i.e.,budbreakphenology)initiatesthegrowingseasonandrepresentsasignificantdriverofecosystemproductivity,soilresourceacquisition,andcarbondynamics(Nord&Lynch,2009;Pol-gar&Primack,2011;Richardsonetal.,2009,2010).Together,theindividuals,populations,andcommunitiesthatpersistalongenviron-mentalgradients,above‐andbelowground,arecentraltounderstand-inghowclimatedrivesevolutionoffunctionalplanttraits,affectsspeciesinteractions,andmayhaveecosystem‐levelconsequences(Hampe&Jump,2011;Kawecki,2008;Woolbrightetal.,2014).Theeffectsofintraspecificvariationonecologicalprocesseshavebeendetectedacrossscalesanddiversetaxonomicgroups(De