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Dispatches
,.,andCheng,K.(2005).compensatesforlongitudinaldisplacementformigratorynavigationintwosongbird
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Evolution:Cleistogamytotherescueofzygomorphic
flowers
HerveSauquet1,2
1NationalHerbariumofNewSouthWales(NSW),RoyalBotanicGardensandDomainTrust,Sydney,NSW2000,Australia
2EvolutionandEcologyResearchCentre,SchoolofBiological,EarthandEnvironmentalSciences,UniversityofNewSouthWales,Sydney,
Australia
Correspondence:herve.******@
/
Cleistogamousflowersneverfullybloomandarethoughttohaveevolvedasameanstopromoteself-
symmetry.
Bisexualityisaremarkablephenomenonhighlyefficientpollinationstrategiesusingextraordinarywaytoincreasethechances
,-fertilisationinabisexualfloweristo
speciesoflandplantsproducebothHowever,,somespeciesof
femaleandmalereproductiveunitsinthecost:theysignificantlyincreasetheriskoffloweringplantsindeedproduceclosed,
sameindividuals,floweringplantsself-
(angiosperms)arenodoubtchampionsofwhyflowershaveinventednumerousfemaleorgansareincloseproximityto
,amajorityofthewaystoavoidself-,referred
approximately400,000extantspeciesofremainingbisexual,includingdichogamytoascleistogamy,haslongbeenknown
floweringplantshavetrulybisexual(separationofsexesintime),herkogamyandhassofarbeendocumentedinat
reproductiveunits,calledflowers,(separationofsexesinspace),
comprisingbothfemale(carpels)andgeneticself-incompatibility1,
male(stamens)organsusuallyYetself-fertilisation,oratleastthethisissueofCurrentBiologynowshows
surroundedbysterileparts(theperianth).potentialforit,maybeagoodthinginthatcleistogamyevolvedmorefrequently
Thisfeaturemaybeoneofthekeystosomecircumstances—forinstancewheninflowerswithbilateralsymmetry
(zygomorphy)aspredictedbyCharles
floweringplantsintermsofbothspecieswhyself-,the
diversityandecologicaldominanceinnumeroustimesinfloweringplantsauthorsassembledalarge,impressive
mostterrestrialhabitats,becauseitisdespiteitspositiveimpactondatasetofcleistogamypresenceandfloral
thoughttohavefacilitatedtheevolutionofdiversificationrates2,,523speciesofflowering
R332CurrentBiology31,R330–R358,April12,2021CrownCopyrightª2021PublishedbyElsevierInc.
ll
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plants(spanning378families,orabout
90%ofallfamiliescurrentlyrecognised)Actinomorphic
andamatchingphylogenetictreeZygomorphic
reconstructedfromavailablesequence
comparativemethodstotestthe
correlationbetweenthetwotraits.
TheresultsofJolyandSchoenwere
unambiguous:whicheverwaythey
analysedtheirdata,theyfoundvery
strongsupportforanassociation
analysis,basedonaBayesianapproach
named‘reversible-jumpMarkovChain
MonteCarlo’,theevolutionarytransition
ratefromnon-cleistogamousto
cleistogamousspecieswasfoundtobe
almostfourtimeshigherinlineageswith
floralbilateralsymmetrycomparedto
Bayesianapproachisparticularly
attractiveforitsabilitytotakeintoaccount
variousformsofuncertainty,itwas
reassuringtoseethatotheranalyses
supportedthesameresults,including
morecomplexmodelsthattookinto
accountthepotentialimpactofbothtraits
Whyaretheseresultssointeresting?
.
TheanswerliesinaconundrumaboutZygomorphy(floralbilateralsymmetry)arosenumeroustimesindependentlyfromactinomorphy(floral
cleistogamy:forcleistogamytoberadialsymmetry)
maintainedinaspeciesoranentirereconstructionofthecharacterontheangiospermphylogeny,usingthemethodsandtreeofSauquet
720
lineage,,aswell
asmostoftheirkeyclades,wereancestrallyactinomorphic(asindicatedbytheyellowpiechartsatthe
(althoughafewexceptionshavebeencenterofthetree)andthatthistraitwasretainedacrossmostofitslineages(yellowbranches
reported4).Inotherwords,cleistogamythroughoutthetree).Italsoillustrateshowzygomorphy(bluecolour)evolvednumeroustimes
isespeciallyadvantageouswhenitindependentlythroughoutflowering-plantevolution,characterisingentireclades(noteblueregionsof
thetree,sometimeswithreversalstoactinomorphy,seenasyellowbranchesnestedinblueregions)or
existsasapolymorphism,wherebysingletaxa(individualbluebranches).Thisreconstructionisbasedonalimitednumberofsampled
bothcleistogamous(closed)andspecies(792intotal)anddoesnotrepresentthecompletehistoryoffloralsymmetryevolution,but
5,7,8
chasmogamous(open)
producedbythesameindividualphotographsfeatureexamplesofzygomorphicflowers(clockwisefromtop):Aristolochiaclematitis
(Aristolochiaceae),Cypripediumcalceolus(Orchidaceae),Strelitziareginae(Strelitziaceae),Grevillea
polymorphismasapolyphenism,juniperina(Proteaceae),Impatiensparasitica(Balsaminaceae),Salviapratensis(Lamiaceae),Lonicera
becausebothtypesofflowersmayetrusca(Caprifoliaceae),Dillwyniafloribunda(Fabaceae),Violatricolor(Violaceae)(photographsby
,,¨nenberger,,).
emergefromthesamegenetic
background,butviadifferent
(Figure1)—atleast130timesaccordingstudieshaveshownasignificant,positive
authorspropose,cleistogamymaybetoapreviousstudy8,andupto142–166associationbetweenzygomorphy(either
)
cross-fertilisationwhenself-fertilisationFurthermore,zygomorphyisanddiversificationrates9,,
ofopenflowersisphysicallycharacteristicofsomeofthelargestzygomorphyalsocomeswithacost:
,includingorchidszygomorphicflowersaregenerally
Zygomorphy(floralbilateralsymmetry,(Orchidaceae)andlegumes(Fabaceae).Athoughttobemorespecialised,inother
alsotermedmonosymmetry)isoneofthekeyadvantageofzygomorphyisthoughtwords,havefewerpotentialpollinators,
mostdistinctivetraitsofthespectaculartobehigherpollinationefficiencythroughthanactinomorphicones(anidea
actinomorphy(floralradialsymmetry,orbodyofanimalpollinators,inparticularmeta-analysisofempiricaldata11).This
polysymmetry)isclearlyancestralinthepositionofanthers(whichdeliverimpliesthatevolvingzygomorphicflowers
floweringplants7,zygomorphyevolvedpollen)andstigmas(whichreceivemaybeariskystrategyfroman
numeroustimesindependentlypollen).Consistentwiththisidea,previousevolutionarypointofview,especially
CurrentBiology31,R330–R358,April12,2021R333
ll
Dispatches
whenthephysicalarrangementofsexualexpressionsofzygomorphy,,.,andKlooster,.(2007).The
organspreventsautonomousdevelopmentalstudieshaverevealedverycleistogamousbreedingsystem:Areviewof
itsfrequency,evolution,andecologyin
self-fertilisation:,1.
ononetypeofpollinator,zygomorphicindifferentlineages8,15–
speciesmaybeathigherriskofextinctionofstatisticalphylogeneticapproaches,,S.,andSchoen,.(2021).Repeated
evolutionofareproductivepolyphenismin
ifthosepollinatorsbecomescarce(eithertheseobservationssuggestthatdifferentplantsisstronglyassociatedwithbilateral
episodicallyorpermanently),,
–1520.
flowersmayevolve(andberetained)However,,.,andLloyd,.(1984).The
morefrequentlyinzygomorphicflowers,symmetry,itisreassuringtoobservethatselectionofcleistogamyandheteromorphic
,303–322.
pollinatorsandarelesscapableofmorphologicaldevelopmentallevel,,H.,vonBalthazar,M.,Magallo´n,S.,
self-fertilisationthanactinomorphicevidencesofarsuggeststhatthesameDoyle,.,Endress,.,Bailes,.,
,E.,Bull-Heren˜u,K.,
Carrive,L.,Chartier,M.,etal.(2017).The
Despitethesemeaningfulresultsandrepeatedlyacrossfloweringplantstoancestralflowerofangiospermsanditsearly
theirextensivedatasetandanalyses,theproducezygomorphicflowers8,18,,16047.
studybyJolyandSchoenhassomeFurthermore,itisusefultopointoutthatit
,E.,Sauquet,H.,andNadot,S.(2016).
,945–964.
(includingthoseoftheauthorofthisthatmatterinastudylikethisone,but
,.(2004).Floralsymmetryaffects
dispatch),.
brieflytofurtherhighlightthesignificanceanexplicitphylogeny(,603–608.
),comparative
theauthors,’Meara,.,Smith,.,Armbruster,.,
Harder,.,Hardy,.,Hileman,.,
(suchasfloraltubesformedbyfusionorofatraitandinsteadtakeintoaccounttheHufford,L.,Litt,A.,Magallo´n,S.,Smith,.,
cohesionofperianthparts),butalsocomplexevolutionarypatternsofetal.(2016).Non-equilibriumdynamicsand
flor