The$Role$of$Dispersal$and$Adaptive$Divergence$in$the$Diversification$and$Speciation$of$ the$Tribe$Brassiceae$and$Genus$Cakile' by$ Charles$George$Willis$ Department$of$Biology$ Duke$University$ ! Date:_______________________! Approved:! ! ___________________________! Kathleen!Donohue,!Supervisor! ! ___________________________! Mark!Rausher! ! ___________________________! John!Willis! ! ___________________________! Paul!Manos! ! ___________________________! Cliff!Cunningham! ! Dissertation$submitted$in$partial$fulfillment$of$ the$requirements$for$the$degree$of$Doctor$ of$Philosophy$in$the$Department$of$ Biology$in$the$Graduate$School$ of$Duke$University$ $ 2013$ ! ! $ $ ! $ ABSTRACT$ The$Role$of$Dispersal$and$Adaptive$Divergence$in$the$Diversification$and$Speciation$of$ the$Tribe$Brassiceae$and$Genus$Cakile' Charles$George$Willis$ Department$of$Biology$ Duke$University$ ! Date:_______________________! Approved:! ! ___________________________! Kathleen!Donohue,!Supervisor! ! ___________________________! Mark!Rausher! ! ___________________________! John!Willis! ! ___________________________! Paul!Manos! ! ___________________________! Cliff!Cunningham! ! An$abstract$of$a$dissertation$submitted$in$partial$ fulfillment$of$the$requirements$for$the$degree$ of$Doctor$of$Philosophy$in$the$Department$of$ Biology$in$the$Graduate$School$of$ Duke$University$ $ 2013$ $ $ $ $ $ $ $ ! $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ $ Copyright$by$ Charles$G.$Willis$ 2013 Abstract $ Adaptation$ is$ central$ to$ our$ understanding$ of$ the$ origin$ of$ biological$ diversity.$ Yet$ whether$ adaptive$ divergence$ promotes$ the$ formation$ of$ new$ lineages$ remains$ poorly$ understood.$ My$ dissertation$ addresses$ the$ role$ of$ adaptive$ divergence$ in$ diversification$ and$ speciation.$ I$ also$ investigate$ an$ alternative$ mechanism:$ dispersal,$ which$ can$ promote$ diversification$ and$ speciation$through$its$effects$on$gene$flow$and$allopatry.$$To$address$the$role$of$ divergent$ adaptation$ and$ dispersal$ in$ the$ process$ of$ diversification,$ I$ combine$ comparative$ methods$ with$ quantitative$ genetics$ to$ characterize$ patterns$ of$ diversification$and$speciation$in$the$tribe$Brassiceae$and$genus$Cakile.$I$start$with$ a$ comparative$ study$ of$ the$ role$ of$ dispersal$ and$ adaptation$ in$ diversification,$ and$then$focus$on$the$role$of$climatic$and$latitudinal$divergence$in$the$processes$ of$adaptive$divergence$and$speciation.$In$general,$I$find$limited$evidence$for$the$ role$of$divergent$adaptation$in$the$evolution$of$intrinsic$reproductive$isolation.$ Diversification$in$the$tribe$Brassiceae$appears$to$be$mediated$by$dispersal$ability,$ while$ in$ the$ genus$ Cakile,$ the$ evolution$ of$ intrinsic$ reproductive$ isolation$ is$ largely$independent$of$ecological$divergence.$Thus,$while$divergent$adaptation$ to$novel$habitats$and$climate$are$likely$occurring$in$Brassiceae,$mediated$in$part$ by$ the$ evolution$ of$ longOdistance$ dispersal,$ the$ evolution$ of$ intrinsic$ genic$ reproductive$ barriers$ appears$ to$ not$ be$ influenced$ by$ adaptation. iv$ ! Dedication$ I$ would$ like$ to$ dedicate$ my$ dissertation$ to$ my$ parents,$ Ann$ and$ Steve$ Willis.$Without$their$support$and$encouragement$the$probability$of$all$of$these$ words$and$figures$coalescing$into$something$readable$would$be$slim$to$none.$I$ would$also$like$to$dedicate$my$dissertation$to$my$grandfather,$George$Willis.$It$ was$you$who$got$me$caught$up$in$this$demandable$thing$they$call$science,$and$ I’ll$never$forget$it.$$! ! ! v$ ! ! Contents Abstract$.........................................................................................................................................$iv$ List$of$Tables$................................................................................................................................$vii$ List$of$Figures$................................................................................................................................$ix$ Acknowledgements$.......................................................................................................................$x$ 1.$$Introduction:$An$Overview$.....................................................................................................$1$ 2.$The$Evolution$of$Dispersal$and$Diversification$in$the$tribe$Brassiceae$(Brassicaceae)$.$14$ 2.1$Introduction$.......................................................................................................................$14$ 2.2$Material$and$Methods$......................................................................................................$23$ 2.3$Results$.................................................................................................................................$42$ 2.4$Discussion$...........................................................................................................................$57$ 3.$Adaptive$divergence$along$a$latitudinal$gradient$of$seasonality$in$the$genus$Cakile$...$64$ 3.1$Introduction$.......................................................................................................................$64$ 3.1$Material$and$Methods$......................................................................................................$67$ 3.3$Results$.................................................................................................................................$71$ 3.4$Discussion$...........................................................................................................................$79$ 4.$ Patterns$ of$ reproductive$ isolation$ in$ the$ genus$ Cakile$ and$ the$ role$ of$ ecological$ divergence$.....................................................................................................................................$88$ 4.1$Introduction$.......................................................................................................................$88$ 4.2$Material$and$Methods$......................................................................................................$97$ 4.3$Results$...............................................................................................................................$112$ 4.4$Discussion$.........................................................................................................................$135$ 4.5$Addendum$.......................................................................................................................$142$ 5.$Reproductive$isolation$in$the$genus$Cakile$in$association$with$latitudinal$divergence $......................................................................................................................................................$145$ 5.1$Introduction$.....................................................................................................................$145$ 5.2$Material$and$Methods$....................................................................................................$153$ 5.3$Results$...............................................................................................................................$157$ 5.4$Discussion$.........................................................................................................................$164$ Appendix$A:$Divergence$in$the$genus$Cakile$along$latitudinal$and$climatic$gradients$..$175$ References$...................................................................................................................................$182$ Biography$....................................................................................................................................$204$ ! ! ! ! ! vi$ $ ! List of Tables Table$1.$Taxonomic$and$fruit$trait$diversity$of$the$tribe$Brassiceae.$....................................$27$ Table$2.$Summary$of$fruit$and$seed$traits$used$in$analyzes.$.................................................$34$ Table$3.$Principle$component$loadings$and$proportion$variance$for$climate$and$altitude$ data$for$the$Brassiceae.$.......................................................................................................$40$ ! Table$4.$Test$of$correlated$evolution$of$fruit$traits$and$habitat.$...........................................$51$ Table$5.$Evolution$of$fruit$and$seed$traits.$...............................................................................$52$ Table$6.$Test$of$correlated$evolution$of$fruit$traits$and$habitat.$...........................................$54$ Table$7.$Correlated$evolution$of$habitat$and$seed$traits.$.......................................................$55$ Table$8.$Correlated$evolution$of$fruit$traits,$range$and$climate$variables.$.........................$56$ Table$ 9.$ Test$ for$ significant$ differences$ in$ speciation$ and$ extinction$ rates$ among$ taxa$ with$different$fruit$traits.$...................................................................................................$59$ ! Table$ 10.$ Means$ of$ bolting$ time,$ flower$ number,$ and$ fruit$ number$ means$ by$ species,$ chamber,$year,$and$subspecies.$.........................................................................................$74$ ! Table$11.$Analysis$of$variance$of$bolting$date.$........................................................................$75$ Table$12.$Analysis$of$variance$of$flower$number.$..................................................................$76$ Table$13.$Analysis$of$variance$of$fruit$number.$......................................................................$77$