Gene?owandnaturalselectionshapespatialpatternsofgenesintreepopulations:implicationsforevolutionaryprocessesandapplicationsVictoriaL.SorkAbstractAcentralquestioninevolutionarybiologyishowgene?owandnaturalselectionshapegeographicpatternsofgenotypicandphenotypicvariation.First,throughstudiesofcontemporarypollenandseedmovement,Sorkhasstudiedhowlimitedgenemovementcreates?ne-scalegeneticstructure,whilelong-distancegene?owpromotesconnectivity.Second,Sorkresearchonspatialpatternsofgeneticvariationhasinvestigatedtheinteractingimpactsofgeographyandclimateongene?owandselection.Third,usingnext-generationgenomictools,sheisnowstudyinggeneticvariationonthelandscapeto?ndinitialevidenceofclimate-associatedlocaladaptationandepigeneticvariationtoexploreitsroleinplantresponsetotheclimate.

IntroductionOverthelasttwentyplusyears,herresearchhasfocusedongene?owandgeographicalpatternsofgeneticvariationatdifferenttemporalandspatialscales.1.Gene?owandnaturalselectionaretwocentral.Usuallyopposing,evolutionaryforces:gene?owdistributes,homogenizes,andmaintainsgeneticvariationthatcanactasthe‘stuffofevolution’,whilenaturalselection

reducesgeneticvariationtothevariantsthatfavorsurvivalandreproduction.2.Howthedynamicsofgenemovementcreategeneticstructure？

Analyzecontemporarygenemovementthroughpollenandseeds.Numerousstudieshaveusedpaternity（親本分析）analysistoassessthedistanceofpollen-mediatedgenedispersalandtheshapeofthedispersalkernel.Thisresearchhasgeneratedempiricaldataandnewmethodstoaddresskeyconceptsthroughthreelinesofinquiry:1

Contemporarygene?owatalandscapescale.

2Geographicpatternsofgeneticvariation.3Landscapegenomicsofadaptivegeneticvariation.IntroductionFigure1(A)PhotoofadultQuercuslobataNee.(B)Landscapeviewoftypicaloaksavanna（稀樹(shù)草原）habitatwithscatteredlargetreesofQ.lobata(lea?esscanopies)andQ.agrifolia(greencanopies).Backgroundandinitialdrivers1、Whethergene?owwouldswampadaptivedivergence？Althoughwecannotruleoutmaternaleffectsorotherfactors,thesestrongphenotypicdifferencesonascalelessthanafewhundredmetersindicatethelocalselectionpressuresintreepopulationscouldbesuf?cientlyintensetoovercomegene?ow,orgenemovementissuf?cientlyrestrictedthatadaptationcanevolveonalocalscale.2、Impactoflandscapealterationongeneticdiversityofforesttreespecies?（景觀改造）Givenevidencethatlandscapefragmentation(破碎)andreductionsinpopulationsizecouldjeopardize（危及）gene?owandconnectivity.Incontrasttotheotherstudiesthatlookedatimmediateimpactsofforest-cuttingpracticesoninsect,bird,andmammalbiodiversity,becauseofthelongevityoftrees,ourprojectwouldnotbeabletomeasurechangesindiversityforatleast50years.Instead,wechosetoinvestigatetheimpactsoncontemporarypollen?owbecauseanychangesingene?owatthepresenttimewouldshapefuturediversity.Contemporarygene?owintreesatalandscapescaleIfgene?owisimpededbylandscapechanges,thenapopulationbecomesisolatedandcandecreaseineffectivesize,whichincreasesriskofinbreedingdepressionandlossofadaptivegeneticvariationthroughdrift.Gene?owwillpromotegeneticdiversitywithinlocalpopulationsandconnectivityamongpopulations.WeeventuallyfocusedourstudiesonthepollenandseeddispersalvectorsofCaliforniapopulationsofvalleyoak,Quercuslobata(Fig.3).Figure3Stagesofplantreproductionofwind-pollinatedandanimal-dispersedQuercuslobatainvolvedingene?ow.Pollenmovement

Pollenmovementinoaksisresponsibleformaintainingconnectivityamongpopulations,yetlocalpollinationissuf?cientlyfrequentthatitispossibletocreate?ne-scalegeneticstructurethatcouldfacilitatelocaladaptation.

Formosttreepopulations,gene?owoccursprimarilythroughpollen.

pollenpooleffectivenumberofpollendonorslong-distancegene?owriskofgeneticdriftlocaladaptationconservationstrategiesSeedmovementatalandscapescale

Seeddispersalismorelikelytoberestricted,soitaccountsformuchmoreofthe?ne-scalegeneticstructurethandoeslocalpollenmovement.Dispersalagents,suchaswesternscrubjays(灌叢鴉),facilitatelong-distanceacornmovementthatwouldallowcolonizationofnewsites,butbecausetheyvisitfewtrees,thegeneticdiversityofpatchyseedlingpopulationsisreducedduringthisphasefromthatintroducedthroughpollendispersal.

Formanytreespeciesisthatlocalizedgenemovementofpollenandseedswillcreatesuf?cientgeneticstructuretoallowtheevolutionoflocaladaptation,whilelong-distancegene?owwillmaintainhighlevelsofgeneticdiversityandspreadfavorableallelesoverlargespatialscales.GeographicpatternsofgeneticvariationGeographicalpatternsofgeneticvariation:

(1)demographichistoryofpopulationexpansionandcontraction(2)migrationhistory(3)naturalselectionbothspatiallyandtemporally1.SpatialautocorrelationThesimplestformofspatialanalysisofgeneticvariationistoexaminethescaleofspatialautocorrelationofalleles.Mostplantpopulationsshowsomedegreeofspatialgeneticstructure(SGS),suggestingthisshortdistancegene?owcreatesopportunityforthesurvivaloflocallyadaptedgeneticvariation.Geographicpatternsofgeneticvariation2.Geographicandenvironmentalassociationswithgeneticgradients(梯度)Whenaspeciesiswidelydistributed,itsevolutionaryhistorycanresultin：

geographicmosaic（鑲嵌）ofgenotypesthatre?ectsthemovementofgenes,theimpactofgeneticbottlenecks,andtheeffectsoflocalselectionpressures.Thisworkpredictsthatthelate21stcenturyclimateconditionscouldleadtoregionalextinctions（滅絕）formanyvalleyoakpopulationsunlesstheyhavepreexistingtoleranceforwarmer,drier,andmoreseasonalclimateenvironments.Infact,forsometreespecies,interventions,suchasassistedmigration,maybenecessary.3.Phylogeography:Phylogeographyisthestudyofgeographicpatternsofgeneticlineages（基因譜系）withthegoalofunderstandinghowthephysicallandscapeandclimatecyclesshapetheevolutionaryhistoryofspecies,theemergenceofnewspecies,andtheextinctionofothers.LandscapegenomicsofadaptivegeneticvariationHerjointlong-termgoalistounderstandthebasicevolutionarybiologyoflocaladaptionintreepopulations,particularlyinresponsetoclimate,andthegeneticcompositionoftreepopulationswillshapetheirresponsetoclimate.1.Climate-associatedcandidategenesIdentified40geneswhinfourfuncionalcategoriesforresponsetoclimatethatcouldbepotentialcandidatesunderselection.First,wefoundthatthetop5%ofFSTestimatesrangedfrom0.25to0.68,whilethemeanFST=0.03.Second,incorrelationanalysesofthe195single-nucleotidepolymorphisms(SNP)frequencieswithclimategradients,wefoundthreeSNPswithinbudburstand?oweringgenesandtwoSNPswithintemperaturestressgenesthatweresigni?cantlyassociatedwithmeanannualprecipitation(Fig.4).Theseanalysesrevealedthat10ofthe40candidategenesshowedevidenceofspatiallydivergentselection.Landscapegenomicsofadaptivegeneticvariation2.EpigeneticdifferentiationinvalleyoakEpigeneticvariationhasthepotentialtoshapephenotypicplasticity(表型可塑性)andadaptationtotheenvironment,eachofwhichcouldbeparticularlyimportantforthepersistenceoflong-livedorganismssuchastrees.ThispotentialisillustratedbystudiesofnaturalpopulationsofArabidopsis

thaliana（擬南芥）thatrevealpatternsofDNAmethylationwhichvaryacrossenvironmentsandmayprovideamechanismtoenhancetheadaptationtothelocalenvironment.ToassesswhethertheSNP(single-nucleotidepolymorphism)andSMP(singlemethylatedsitepolymorphism)variationdiffersacrosspopulations,wecalculatedpopulationdifferentiation,FST.Plattetal.(2015)foundthatmeanepigeneticdifferentiationamongthreepopulationsatvariablymethylatedCGsites(CG-SMPs)washigherthanthatbasedonSNPs(FST=0.28versusFST=0.19