Early Flowers and Angiosperm Evolution Therecentdiscoveryofdiversefossilflowersandfloralorgans inCretaceousstratahasrevealedastonishingdetailsaboutthe structural and systematic diversity of early angiosperms. Exploring the rich fossil evidence that has been accumulated over the past three decades, this unique study follows the evolutionary history of flowering plants from their earliest phasesinobscuritytotheirdominanceinmodernvegetation. The book provides comprehensive biological and geological background information, before moving on to summarise the fossilrecordindetail.Includingpreviouslyunpublishedresults based on research into Earlyand Late Cretaceous fossil floras from Europe and North America, the authors draw together direct palaeontological evidence of the pattern of angiosperm evolutionthroughtime. Synthesising palaeobotanical data with information from livingplants,thisbookexploresthelatestresearchinthefield and highlights connections with phylogenetic systematics aswellasthestructureandthebiologyofextantangiosperms. Else Marie Friis isintheDepartmentofPalaeobotanyatthe Swedish Museum of Natural History. Her research interests includeCretaceousflowersandotherfossilreproductivestruc- tures,withparticularfocusontheoriginandearlydiversification ofangiospermsandrelatedseedplants. Peter R. Crane is in the School of Forestry and Environ- mentalStudiesatYaleUniversity.Hisresearchinterestsinclude large-scale patterns and processes of plant evolution and integrated palaeobotanical and neobotanical studies of plant diversityandevolution. Kaj Raunsgaard Pedersen is in the Department of Geology at the Universityof Aarhus. His research interests include integrated palynological and palaeobotanical studies ofMesozoicseedplantswithparticularfocusonCretaceous reproductivestructuresandfloweringplantevolution. Early Flowers and Angiosperm Evolution Else Marie Friis Swedish Museum of Natural History, Stockholm Peter R. Crane School of Forestry & Environmental Studies, Yale University Kaj Raunsgaard Pedersen Department of Geology, University of Aarhus Line drawings by Pollyanna von Knorring cambridge university press Cambridge,NewYork,Melbourne,Madrid,CapeTown,Singapore, Sa˜oPaulo,Delhi,Tokyo,MexicoCity CambridgeUniversityPress TheEdinburghBuilding,CambridgeCB28RU,UK PublishedintheUnitedStatesofAmericabyCambridgeUniversityPress,NewYork www.cambridge.org Informationonthistitle:www.cambridge.org/9780521592833 #E.M.Friis,P.R.CraneandK.R.Pedersen2011 Thispublicationisincopyright.Subjecttostatutoryexception andtotheprovisionsofrelevantcollectivelicensingagreements, noreproductionofanypartmaytakeplacewithout thewrittenpermissionofCambridgeUniversityPress. Firstpublished2011 PrintedintheUnitedKingdomattheUniversityPress,Cambridge AcataloguerecordforthispublicationisavailablefromtheBritishLibrary LibraryofCongressCataloging-in-PublicationData Friis,ElseMarie. Earlyflowersandangiospermevolution/ElseMarieFriis,PeterR.Crane, KajRaunsgaardPedersen. p. cm. ISBN978-0-521-59283-3(Hardback) 1. Angiosperms,Fossil. 2. Angiosperms–Evolution. I. Crane,PeterR. II. Pedersen,KajRaunsgaard. III. Title. QE980.F752011 561–dc22 2011001815 ISBN978-0-521-59283-3Hardback CambridgeUniversityPresshasnoresponsibilityforthepersistenceor accuracyofURLsforexternalorthird-partyinternetwebsitesreferredto inthispublication,anddoesnotguaranteethatanycontentonsuch websitesis,orwillremain,accurateorappropriate. Contents Preface pageix 5 Angiospermsincontext:extantandfossil seedplants 101 1 Introductiontoangiosperms 1 5.1 Angiospermsamongextantandfossil 1.1 Phylogeneticpositionofangiosperms 1 seedplants 101 1.2 Characteristicfeaturesofangiosperms 6 5.2 Bennettitales–Erdtmanithecales–Gnetales 1.3 Timingofangiospermdiversification 16 (BEG)group 104 1.4 Risetoecologicaldominance 19 5.3 Gnetales 105 5.4 Erdtmanithecales 114 2 Thenatureoftheangiospermfossil 5.5 Unassigneddispersedseedsofthe record 23 BEGgroup 119 2.1 Understandingtheplantfossilrecord 23 5.6 Bennettitales(Cycadeoidales) 124 2.2 Theadequacyoftheangiospermfossil 5.7 Pentoxylales 130 record 38 5.8 OtherPalaeozoicandMesozoicseedplants 131 3 Theenvironmentalcontextofearly 6 Originandageofangiosperms 141 angiospermevolution 39 6.1 Hypothesesofseedplantrelationships 141 3.1 Palaeogeography 39 6.2 Originofangiospermstructure 150 3.2 Palaeoclimate 45 6.3 Theageofangiosperms 155 3.3 Climatechangeduringthe 6.4 Pre-Cretaceousangiosperm-likefossils 158 Cretaceous 50 3.4 Implicationsforangiosperm 7 Phylogeneticframeworkandthe diversification 53 assignmentoffossilstoextantgroups 163 7.1 Earlyideasonangiospermphylogeny 163 4 Stratigraphicframeworkandkeyareas 7.2 Phylogeneticstudiesofangiospermsbasedon forCretaceousangiosperms 55 moleculardata 163 4.1 Thestratigraphicframework 55 7.3 Angiospermphylogenygroupclassification 4.2 KeyareasforCretaceousangiosperms 56 (APGIII) 164 4.3 Europe 57 7.4 Angiospermphylogeny:futuredirections 167 4.4 EasternNorthAmerica 72 7.5 Assignmentoffossilstoextantgroups 168 4.5 WesternInterioroftheUnitedStates andCanada 79 8 Fossilsnearthebaseoftheangiospermtree 169 4.6 Alaska 81 8.1 Early-divergingangiospermlineagesatthe 4.7 Greenland 82 ANITAgrade 169 4.8 Israel,JordanandLebanon 82 8.2 Amborellaceae 171 4.9 NorthAfrica 84 8.3 Nymphaeales 171 4.10 WestAfricaandBrazil 85 8.4 Austrobaileyales 176 4.11 Asia 88 8.5 Chloranthaceae 180 4.12 SouthernGondwanaandIndia 96 8.6 Ceratophyllaceae 185 v vi Contents 9 Earlyfossilangiospermsofuncertain 13.7 Caryophyllales 315 relationships 189 13.8 Saxifragales 316 9.1 Putativeangiosperms 189 9.2 Fossilflowersattachedtoinflorescences 14Fossilsofcoreeudicots:rosids 327 andstems 192 14.1 Classificationofrosids 327 9.3 Isolatedflowersandfruitspreservedas 14.2 Fossilevidenceofrosids 327 compressions/impressions 200 14.3 Vitales 329 9.4 Permineralisedflowers 201 14.4 Fabids(EurosidsI) 329 9.5 Isolatedangiospermmesofossils 202 14.5 TheCOMclade 329 9.6 Dispersedmonoaperturatepollen 208 14.6 Thenitrogen-fixingclade 332 9.7 Fossilleavesofuncertainrelationships 215 14.7 Malvids(EurosidsII) 354 10Earlyfossilsofeumagnoliids 219 15Earlyfossilsofeudicots:asterids 361 10.1 Classificationofeumagnoliids 219 15.1 Classificationofasterids 361 10.2 Magnoliales 223 15.2 Cornales 363 10.3 Laurales 231 15.3 Ericales 365 10.4 Canellales 244 15.4 Lamiids(EuasteridsI) 378 10.5 Piperales 246 15.5 Boraginaceae,IcacinaceaeandVahliaceae 379 15.6 Garryales 381 11Fossilsofmonocots 249 15.7 Gentianales 381 11.1 Classificationofmonocots 249 15.8 SolanalesandLamiales 382 11.2 Fossilevidenceofmonocotdiversification 250 15.9 Campanulids(EuasteridsII) 382 11.3 Putativeearlymonocotfossils 250 15.10 Aquifoliales,EscallonialesandAsterales 383 11.4 Acorales 255 15.11 Bruniales,Apiales,Paracryphialesand 11.5 Alismatales 256 Dipsacales 385 11.6 Dioscoreales 266 11.7 Pandanales 266 16Patternsofstructuraldiversificationin 11.8 Liliales 267 angiospermreproductiveorgans 387 11.9 Asparagales 267 16.1 Inflorescencestructure 388 11.10 Commelinids 268 16.2 Floralorganisation 391 12Fossilsofeudicots:early-diverginggroups 275 16.3 Otheraspectsoffloralconstruction 412 12.1 Classificationofeudicots 275 12.2 Early-divergingeudicots 276 17Historyandevolutionofpollinationin 12.3 Fossilevidenceofeudicotdiversification 277 angiosperms 415 12.4 Fossilsofuncertainrelationships 277 17.1 Pollinationinextantnon-angiospermseed 12.5 Ranunculales 289 plants 415 12.6 Proteales 292 17.2 Pollinationinextantangiosperms 417 12.7 Sabiaceae 301 17.3 Insectsaspollinators 419 12.8 Buxales 303 17.4 Vertebratesaspollinators 426 12.9 Trochodendrales 308 17.5 Historyofpollinationinangiosperms 428 17.6 Large-scaletrendsinthehistoryof 13Fossilsofcoreeudicots:basallineages 311 angiospermpollination 441 13.1 Classificationofcoreeudicots 311 13.2 Earlyfossilevidenceofcoreeudicots 312 18Historyandevolutionofdispersalin 13.3 Gunnerales 312 angiosperms 445 13.4 Dilleniaceae 313 18.1 Dispersalinextantnon-angiosperm 13.5 Berberidopsidales 313 seedplants 445 13.6 Santalales 314 18.2 Dispersalinextantangiosperms 447 Contents vii 18.3 Animaldispersers 448 20Theaccumulationofangiospermdiversity 475 18.4 Historyofdispersalinangiosperms 450 20.1 Large-scalepatternsinangiosperm 18.5 Large-scaletrendsinthehistoryof diversification 475 angiospermdispersal 456 20.2 Patternsofangiospermdiversification:early lineages 477 19Vegetationalcontextofearlyangiosperm 20.3 Patternsofangiospermdiversification: diversification 461 eumagnoliids 483 19.1 Transitiontoangiosperm-dominated 20.4 Patternsofangiospermdiversification: vegetation 461 monocots 486 19.2 ComponentsofEarlyCretaceous 20.5 Patternsofangiospermdiversification: vegetation 462 eudicots 488 19.3 Vegetationduringtheearlydiversification 20.6 Angiospermevolutionandglobalchange ofangiosperms 467 throughtheCenozoic 495 19.4 Earlyangiosperms:diversityinobscurity 469 20.7 Prospects 498 19.5 Mid-Cretaceousvegetation 471 19.6 LateCretaceousvegetationandfloristic References 501 provinces 472 Index 573 Preface Developmentsinthestudyoffossilandlivingplantsover standard approaches to Cenozoic fossil floras in Europe, thepastfewdecadeshavegreatlyclarifiedmanyaspectsof and pioneered in the Late Cretaceous of Scania, Sweden, earlyangiospermevolution.Explicitphylogeneticanalyses, have now yielded diverse angiosperm flowers from many facilitatedbythedevelopmentofcomputertechnologyand new fossil floras (mesofossil floras) discovered in Lower based on both morphological and molecular data, have and Upper Cretaceous strata in Europe, North America, renewed interest in the relationships of angiosperms to Asia,NewZealandandAntarctica. other plants, the patterns of relationship among major In this book we provide a synthesis and overview of groupsofangiosperms,andtheprocessesthathavegener- currentdataandideasonthemajorpatternsofangiosperm ated angiosperm diversity at both microevolutionary and evolution,focusingespeciallyontheearlyevolutionofthe macroevolutionary scales.At thesame time, arapid accu- group. Our emphasis is on the new information from mulationofnewinformationonthestructureandbiology the fossil record that has accumulated over the past three of many key groups of living angiosperms has catalysed decades and how this relates to recent findings on the comparative studies and brought tolight many previously phylogenetic systematics, structure and biology of extant unrecognised features that provide new perspectives on angiosperms.Centraltothissynthesisofthepalaeobotani- angiospermevolution. cal data is its integration with information from living Palaeobotanicalstudieshavealsobeencentralinrevital- plants and the presentation of previously unpublished ising research on early angiosperm evolution and have results based on our research with Early and mid- advanced significantly our understanding of early angio- Cretaceous fossil floras from eastern North America and sperm history. In particular, the discovery of diverse and Portugal. exquisitelypreserved fossil flowers andfloralorgans from Chapters1to4providethebackgroundtoinformation the Cretaceous has yielded detailed information on the and ideas discussed in more detail later in the book. structural and systematic diversity of early angiosperms. Chapter 1 introduces recent developments in angiosperm These data complement the information available from palaeobotany, molecular systematics and studies of the livingplants,andarealsoinvaluablefortestingevolution- flowers of livingplants, and brieflyconsiders some of the aryhypothesesbasedonextanttaxaagainstpalaeobotanical waysinwhichtheseadvancesarechangingourperspective andstratigraphicevidence.Therecognitionoffossilpollen on early angiosperm evolution. Major features of angio- grainsinsituwithinflowershasalsoprovidednewpossibil- sperm structure and biology are also reviewed along with ities for interpreting the record of dispersed fossil pollen. previous ideas on the origin and earlyevolution of angio- Onlya fewdecades agothe abundant occurrence of fossil spermsandtheirflowers,aswellastheriseofangiosperms angiosperm flowers in Cretaceous strata was unimagined, toecologicaldominance.Chapter2providesanoverviewof buttodaythereisarichfloralrecord,muchofwhichstill the nature of the angiosperm fossil record. Chapter 3 remainstobeanalysedindetail.Thekeybreakthroughwas briefly outlines changes in palaeogeography and climate the recognition that numerous small fossil flowers, which since the Early Cretaceous, as an introduction to the are generally not visible to collectors in the field, can be changing world in which angiosperm diversification took extractedfromCretaceoussedimentsbyusingbulk-sieving place.Chapter 4brieflydiscussesthestratigraphicframe- techniques and studied with scanning electron micros- workandoccurrenceoftheangiospermfossilsconsidered copy(SEM),andnowalsowithsynchrotronX-raymicro- in this book and provides a review of the key fossil tomography (SXRTM). These techniques, modified from localities. ix