The choanoflagellates : evolution, biology and ecology

332 Pages·2014·39.656 MB·English

by  Leadbeater, Barry S. C

The Choanoflagellates
Evolution, Biology and Ecology
Choanoflagellates have three distinctive claims to fame: they are
theclosest,living,unicellularrelativesofanimals;theyareamajor
component of aquatic microbial foodwebs; and one group is
remarkableforitssiliceousbasket-likecoverings.
Thislandmarkbookoffersauniquesynthesisofover40years
of choanoflagellate research. Key areas are covered, from the
phylogenetic evidence supporting the sister-group relationship
betweenchoanoflagellatesandMetazoa,tochoanoflagellatedistri-
butionanddiversityinmarineandfreshwaterenvironments.The
structure and assembly of choanoflagellate loricae is also pre-
sented together with a full discussion of a novel example of
‘regulatoryevolution’,suggestingthattheswitchfromnudiform
totectiformcelldivisionandloricaproductionwasachievedbya
suddenreorganisationofexistingstructuresandmechanisms.
Providinganauthoritativesummaryofwhatiscurrentlyknown
aboutchoanoflagellates,thistitlewillserveasafoundationupon
whichfutureresearchanddiscussioncantakeplace.
BARRYS. C. LEADBEATER isaretiredReaderinProtistologyat
the University of Birmingham. His academic research interests
include: ultrastructure, physiology and ecology of algae and
protozoa,whereashisbiotechnologicalresearchinterestsinclude:
algaeandwaterquality,physiologyofalgal/protistanbiofilmsand
biologicalaspectsofwater treatmentprocesses.Hehasauthored
andco-authoredover80papers,editedfivebooksand,presently,
heisamonitoringeditorofthejournalProtist.

The Choanoflagellates
Evolution, Biology and Ecology
Barry S. C. Leadbeater
University of Birmingham, UK
UniversityPrintingHouse,CambridgeCB28BS,UnitedKingdom
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www.cambridge.org
Informationonthistitle:www.cambridge.org/9780521884440
©BarryS.C.Leadbeater,2015
Thispublicationisincopyright.Subjecttostatutoryexception
andtotheprovisionsofrelevantcollectivelicensingagreements,
noreproductionofanypartmaytakeplacewithoutthewritten
permissionofCambridgeUniversityPress.
Firstpublished2015
PrintedintheUnitedKingdombyTJInternationalLtd.PadstowCornwall
AcataloguerecordforthispublicationisavailablefromtheBritishLibrary
LibraryofCongressCataloginginPublicationData
Leadbeater,BarryS.C.
Thechoanoflagellates:evolution,biology,andecology/BarryS.C.Leadbeater,UniversityofBirmingham,UK.
pages cm.
Includesbibliographicalreferencesandindex.
1. Choanoflagellates. 2. Protozoa. I. Title.
QL368.C5L432014
579.4–dc23 2014022201
ISBN978-0-521-88444-0Hardback
CambridgeUniversityPresshasnoresponsibilityforthepersistenceoraccuracyof
URLsforexternalorthird-partyinternetwebsitesreferredtointhispublication,
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Contents
Preface pageix
NoteonTerminology,TaxonomyandNomenclature xii
1 Historicalperspectives 1
1.1 Introduction 1
1.2 Firstpublishedrecordofacollar-bearingflagellate 1
1.3 Morphologyandreproductionofthe‘collaredflagellate’ 4
1.4 ChoanoflagellatesasancestorsofthespongesandlowerMetazoa 10
1.5 Haeckel’sGastraeatheoryandoriginofthelowerMetazoa(non-Bilateria) 13
1.6 Alternativetheoriesofmetazoanevolutioninvolvingchoanoflagellateancestors 14
1.7 The‘collarcell’asadistinctivecelltype 14
1.8 Choanoflagellateclassification 15
2 Thecollaredflagellate:functionalmorphologyandultrastructure 18
2.1 Functionalmorphology:introduction 18
2.2 Thehydrodynamicenvironmentofchoanoflagellates 18
2.3 Modellingwaterflowinresponsetoflagellaractivity 19
2.4 Particlecaptureandingestion 26
2.5 Ultrastructure:introduction 28
2.6 Theflagellarapparatus 28
2.7 Cytoskeleton 32
2.8 Cytoplasmicorganelles 37
2.9 Nucleusandnucleardivision(mitosis) 40
3 Craspedida:choanoflagellateswithexclusivelyorganiccoverings 44
3.1 Introduction 44
3.2 CellcycleoftheCraspedida 44
3.3 Specieswithnon-restrictivecellcoverings 44
3.4 Specieswithrestrictivecellcoverings 47
3.5 Colonialchoanoflagellates 54
3.6 Encystment 61
3.7 Discussion 63
4 Loricatechoanoflagellates:Acanthoecida 66
4.1 Introduction 66
4.2 Terminologyandpreservationofchoanoflagellateloricae 67
4.3 Loricaconstruction 70
4.4 Evidenceforauniversalleft-handedrotationinloricaconstruction 82
4.5 Organiccomponentsofloricae 83
4.6 Variationsonthemes 85
v
vi Contents
4.7 Discussion 98
4.8 ‘Rules’ofloricaconstructionandassembly 99
5 Loricatechoanoflagellates:requirementforsiliconanditsdepositionincostalstrips 100
5.1 Introduction 100
5.2 Biogeochemicalcyclingofsiliconinseawater 101
5.3 Terminology 102
5.4 Stephanoecadiplocostata:theexperimentalspecies 102
5.5 UltrastructureofcostalstripproductioninStephanoecadiplocostata 104
5.6 Effectsofmicrotubulepoisonsonthecytoskeletonandcostalstripdevelopment 108
5.7 GrowthandsiliconturnoverinStephanoecadiplocostata 112
5.8 Discussion 126
6 Loricatechoanoflagellates:Acanthoecidae–nudiformspecies 130
6.1 Introduction 130
6.2 Terminology:spiralsandhelices 132
6.3 Nudiformchoanoflagellates(Acanthoecidae) 132
6.4 Savillea 133
6.5 Helgoeca 138
6.6 ThePolyoeca–Acanthoecacontinuum 140
6.7 Logisticalandmechanicalaspectsofloricaassembly 147
6.8 Roleofthecytoskeletonduringloricaassembly 147
6.9 Evolutionarysignificanceofnudiformchoanoflagellates 153
7 Loricatechoanoflagellates:Stephanoecidae–tectiformspecies 155
7.1 Introduction 155
7.2 Stephanoecadiplocostata 156
7.3 Didymoecacostata 166
7.4 Diaphanoecagrandis 175
7.5 Featuresthatcharacterisethetectiformcondition 179
7.6 Universalityoffeaturescharacteristicoftectiformdivision 181
7.7 Aretransversecostaeanexclusivelytectiformfeature? 183
8 Loricatechoanoflagellates:evolutionaryrelationshipbetweenthenudiformandtectiformconditions 185
8.1 Introduction:anevolutionaryparadox 185
8.2 Background 185
8.3 Thenudiformcondition 185
8.4 Thetectiformcondition 187
8.5 Codifyingthesalientfeaturesofthenudiformandtectiformconditions 191
8.6 Onejumpevolutionorgradualchange? 192
8.7 Evolutionaryimplicationsoftherelationshipbetweenthenudiformandtectiformconditions 199
9 Choanoflagellateecology 202
9.1 Introduction 202
9.2 Systematicandfunctionaldiversityofheterotrophicflagellates 203
9.3 Ecophysiologyofchoanoflagellates 204
9.4 Ecologyofmarineandbrackishwaterchoanoflagellates 213
9.5 VariabilityinloricasizeofBicostaandCalliacanthaspecies 233
9.6 Functionalroleofchoanoflagellateloricae 236
9.7 Ecologyoffreshwaterchoanoflagellates 237
9.8 Conclusions 240
Contents vii
10 Choanoflagellatephylogeny:evolutionofmetazoanmulticellularity 241
10.1 Introduction 241
10.2 PhylogenyofOpisthokonta:morphologicalandmolecularperspectives 243
10.3 Opisthokontclassification 249
10.4 Holozoa 251
10.5 Nucletmycea 261
10.6 Opisthokontevolution:aconsensusbetweenmorphologyandmolecularphylogeny? 262
10.7 Estimateddatingofopisthokontdiversification 263
10.8 Evolutionofmetazoanmulticellularity 264
10.9 Cell–cellandcell–matrixadhesion 265
10.10 Cell–cellsignallingtransductionpathways 269
10.11 Discussion 276
Glossary 278
References 280
Figureandtablecredits 305
Choanoflagellatespeciesindex 307
Otherspeciesindex 309
Generalindex 311