! RICE UNIVERSITY VARIATION IN SPECIES INTERACTIONS AND THEIR EVOLUTIONARY CONSEQUENCES by Scott Chamberlain A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE Doctor of Philosophy APPROVED, THESIS COMMITTEE Jennifer A. Rudgers, Co-Chair Associate Professor Ecology and Evolutionary Biology Kenneth D. Whitney, Co-Chair Associate Professor Ecology and Evolutionary Biology Volker H.W. Rudolf Associate Professor Ecology and Evolutionary Biology Dennis D. Cox Professor Statistics HOUSTON, TEXAS May 2012 ! ! ! ABSTRACT VARIATION IN SPECIES INTERACTIONS AND THEIR EVOLUTIONARY CONSEQUENCES by Scott Chamberlain Species'interactions'restrict'or'promote'population'growth,'structure'communities,'and' contribute'to'evolution'of'diverse'taxa.'I'seek'to'understand'how'multiple'species' interactions'are'maintained,'how'human'altered'species'interactions'influence' evolution,'and'explore'factors'that'contribute'to'variation'in'species'interactions.'In' Chapter'1,'I'examine'how'plants'interact'with'multiple'guilds'of'mutualists,'many'of' which'are'costly'interactions.'The'evolution'of'traits'used'to'attract'different'mutualist' guilds'may'be'constrained'due'to'ecological'or'genetic'mechanisms.'I'asked'if'two'sets' of'plant'traits'that'mediate'interactions'with'two'guilds'of'mutualists,'pollinators'and' ant'bodyguards,'were'positively'or'negatively'correlated'across'36'species'of'Gossypium) (cotton).'Traits'to'attract'pollinators'were'positively'correlated'with'traits'to'attract'ant' bodyguards.'Rather'than'interaction'with'one'mutualist'guild'limiting'interactions'with' another'mutualist'guild,'traits'have'evolved'to'increase'attraction'of'multiple'mutualist' guilds'simultaneously.'In'Chapters'2'and'3,'motivated'by'the'fact'that'agriculture'covers' nearly'50%'of'the'global'vegetated'land'surface,'I'explore'the'consequences'of'changes' in'plant'mutualist'and'antagonist'guilds'in'agriculture'for'selection'on'plant'traits.'I'first' explore'how'agriculture'alters'abundance'and'community'structure'of'mutualist' ! ! ! pollinators'and'antagonist'seed'predators'of'wild'Helianthus)annuus)texanus.'Mutualists' were'more'abundant'near'crops,'whereas'antagonists'were'more'abundant'far'from' crops'near'natural'habitat.'In'addition,'mutualist'pollinator'communities'were'more' diverse'near'sunflower'crops.'Plant'mutualists'and'antagonists'respond'differently'to' agriculture.'Next,'I'explore'how'these'changes'in'abundance'and'community'structure' of'mutualists'and'antagonists'influenced'natural'selection'on'H.)a.)texanus'floral'traits.' Natural'selection'on'heritable'floral'traits'differed'near'versus'far'from'crop'sunflowers,' and'overall'selection'was'more'heterogeneous'near'crop'sunflowers.'Furthermore,' mutualist'pollinators'and'antagonist'seed'predators'mediated'these'differences'in' selection.'Finally,'in'Chapter'4,'I'ask'if'variation'in'interaction'outcomes'differs'across' types'of'species'interactions.'Furthermore,'I'examined'the'relative'importance'of' factors'that'create'contextOdependency'in'species'interactions.'Using'metaOanalysis'of' 353'papers,'we'found'that'mutualisms'were'more'likely'to'change'sign'of'the' interaction'outcome'when'compared'across'contexts'than'competition,'and'predation' was'the'least'likely'to'change'sign.'Overall,'species'identity'caused'the'greatest'variation' in'interaction'outcomes:'whom)you'interact'with'is'more'important'for'contextO dependency'than'where)or'when)the'interaction'occurs.'Additionally,'the'most' important'factors'driving'contextOdependency'differed'significantly'among'species' interaction'types.'Altogether,'my'work'makes'progress'in'understanding'how'species' maintain'interactions'with'multiple'guilds'of'mutualists,'how'agriculture'alters'species' interactions'and'subsequent'natural'selection,'and'the'variation'in'species'interaction' outcomes'and'their'causes.! ! ! Acknowledgments I!would!like!to!thank!many!people!for!field!and!laboratory!assistance,!or! facilitating!field!or!lab!work:!Yosuke!Akiyama,!Loren!Albert,!Wael!Al>Wawi,!Rameez! Anwar,!Morgan!Black,!Sean!Campbell,!Charles!Danan,!Neha!Deshpande,!James! Frelichowski,!Alex!Gorischek,!Toby!Liss,!Janna!Love,!Edward!Realzola,!Randall!Ross,!Liz! Seifert,!Rohini!Sigireddi,!and!Prudence!Sun.!Thanks!to!Jonathan!Wendel!for!help!on! construction!of!the!Gossypium!phylogeny.!Thanks!to!the!following!people!for!comments! and!help!on!manuscripts:!Jennifer!Rudgers,!Ken!Whitney,!and!Elizabeth!Elle.!I!am! grateful!to!my!advisors,!Jennifer!Rudgers!and!Ken!Whitney,!for!their!unwavering! support!and!guidance!through!the!duration!of!this!thesis!work.!I!am!indebted!to!my! committee!members!Volker!Rudolf!and!Dennis!Cox!for!their!support!throughout!this! thesis.!Thanks!to!all!the!grad!students!in!the!Ecology!and!Evolutionary!Biology! Department!for!their!advice,!support,!and!encouragement.!I!was!supported!by!a!very! small,!but!gracious!grant!from!the!Biotic!Research!Foundation,!and!by!generous! financial!support!by!my!advisors.!My!loved!ones!made!this!possible!by!providing! emotional!support:!Jeff!and!Janet!Chamberlain,!and!Katherine!Horn.! ! ! ! Contents Acknowledgments........................................................................................................iv' Contents........................................................................................................................v' List.of.Figures..............................................................................................................viii' List.of.Tables..................................................................................................................x' 1..How.do.plants.balance.multiple.mutualists?.Correlations.among.traits.for.attracting. protective.bodyguards.and.pollinators.in.cotton.(Gossypium)........................................1' 1.1.'Abstract'..........................................................................................................................'1' 1.2.'Introduction'...................................................................................................................'2' 1.3.'Materials'and'Methods'..................................................................................................'5' 1.4.'Results'..........................................................................................................................'13' 1.5.'Discussion'....................................................................................................................'15' 1.6.'Conclusion'....................................................................................................................'19' 1.7.'Acknowledgements'......................................................................................................'19' 1.8.'References'...................................................................................................................'20' 1.9.'Tables'...........................................................................................................................'28' 1.10.'Figures'........................................................................................................................'30' 1.11.'Appendix'A'.................................................................................................................'32' 1.12.'Appendix'B'.................................................................................................................'34' 1.13.'Appendix'C'.................................................................................................................'35' 1.14.'Appendix'D'.................................................................................................................'40' 2..Proximity.to.agriculture.alters.abundance.and.community.structure.of.wild.sunflower. mutualists.and.antagonists..........................................................................................41' 2.1.'Abstract'........................................................................................................................'41' 2.2.'Introduction'.................................................................................................................'42' 2.3.'Materials'and'Methods'................................................................................................'45' 2.4.'Results'..........................................................................................................................'55' 2.5.'Discussion'....................................................................................................................'61' 2.6.'Conclusion'....................................................................................................................'66' ! vi! ! 2.7.'Acknowledgements'......................................................................................................'67' 2.8.'References'...................................................................................................................'67' 2.9.'Tables'...........................................................................................................................'75' 2.10.'Figures'........................................................................................................................'76' 2.11.'Appendix'A'.................................................................................................................'81' 3..Proximity.to.crop.sunflowers.affects.patterns.of.natural.selection.in.a.wild.relative. through.plant.mutualists.and.antagonists....................................................................83'