Floral Specialization and Angiosperm Diversity: Phenotypic Divergence, Fitness Trade-offs, and ...

76 Pages·2014·0.52 MB·English

Invited Review
Floral specialization and angiosperm diversity:
D
o
w
phenotypic divergence, fitness trade-offs and realized n
lo
a
d
e
pollination accuracy d
fro
m
h
W. Scott Armbruster1,2,3* ttp
s
1 SchoolofBiologicalSciences,UniversityofPortsmouth,PortsmouthPO12DY,UK ://a
2 InstituteofArcticBiology,UniversityofAlaskaFairbanks,Fairbanks,AK99775-7000,USA ca
d
3 DepartmentofBiology,NorwegianUniversityofScience&Technology,TrondheimN-7491,Norway e
m
Received:4November2013;Accepted:5January2014;Published:16January2014 ic.o
u
Citation:ArmbrusterWS.2014.Floralspecializationandangiospermdiversity:phenotypicdivergence,fitnesstrade-offsandrealized p
.c
pollinationaccuracy.AoBPLANTS6:plu003;doi:10.1093/aobpla/plu003 o
m
/a
o
b
Abstract. Plantreproductionbymeansofflowershaslongbeenthoughttopromotethesuccessanddiversification pla
ofangiosperms.Itremainsunclear,however,howthissuccesshascomeabout.Doflowers,andtheircapacitytohave /a
specializedfunctions,increasespeciationratesordecreaseextinctionrates?Isfloralspecializationfundamentalor rticle
incidental to the diversification? Some studies suggest that the conclusions we drawabout the role of flowers in -a
b
s
thediversificationandincreasedphenotypicdisparity(phenotypicdiversity)ofangiospermsdependsonthesystem. tra
Fororchids,forexample,specializedpollinationmayhaveincreasedspeciationrates,inpartbecauseinmostorchids ct/d
pollenispackedindiscreteunitssothatpollinationispreciseenoughtocontributetoreproductiveisolation.Inmost oi/1
plants,however,granularpollenresultsinlowrealizedpollinationprecision,andthuskeyinnovationsinvolvingflowers 0
.1
morelikelyreflectreducedextinctionratescombinedwithopportunitiesforevolutionofgreaterphenotypicdisparity 09
3
(phenotypicdiversity)andoccupationofnewniches.Understandingthecausesandconsequencesoftheevolutionof /a
o
specializedflowersrequiresknowledgeofboththeselectiveregimesandthepotentialfitnesstrade-offsinusingmore b
p
thanonepollinatorfunctionalgroup.Thestudyoffloralfunctionandflowering-plantdiversificationremainsavibrant la/p
evolutionaryfield.Applicationofnewmethods,frommeasuringnaturalselectiontoestimatingspeciationrates,holds lu0
0
much promise for improving our understanding of the relationship between floral specialization and evolutionary 3
/1
success. 5
6
1
9
6
Keywords: Adaptiveaccuracy;Collinsia;Dalechampia;fitnesstrade-offs;Pedicularis;pollination;realizedprecision; b
y
Stylidium. g
u
e
s
group’sevolutionarysuccessremainelusive(Crepetand t o
Introduction n
Niklas2009).Byevaluatingbotholdandnewideasand 2
0
Flowering plants are the most abundant and diverse identifyingpossiblemisconceptions,thefollowingreview A
p
autotrophicorganismsonland.Reproductionbymeans attempts to come to grips with the role of pollinators, ril 2
0
offlowersandfruitsisofteninvokedasoneofthemain flowers and their interactions inthe diversification and 1
9
causes of this evolutionary success (Stebbins 1974; evolutionarysuccessofplants.
Regal1977),butthemechanismsoftheputativecausal Theevolutionarysuccessandecologicaldominanceof
link between various angiosperm innovations and the angiosperms have been associated with a number of
*Correspondingauthor’se-mailaddress:[email protected]
PublishedbyOxfordUniversityPressonbehalfoftheAnnalsofBotanyCompany.
ThisisanOpenAccessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense(http://creativecommons.org/
licenses/by/3.0/),whichpermitsunrestrictedreuse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited.
AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014 1
Armbruster—Floralspecializationandangiospermdiversity
features.Perhapsmostofteninvokedistheiruseofani- perhaps,flowersinfloweringplants(e.g.Simpson1944,
mals to transport pollen between flowers. The capacity 1953;HodgesandArnold1995;Hunter1998).
of extremespecializationin flowerformand functionis There are three distinct processes that can lead to
thought to have increased diversification rates (Grant differences in evolutionary success in association
1949; Crepet and Niklas 2009) and increased the range with key innovations(phenotypes), the first of which is
ofpollenandseeddispersal,openingnewopportunities microevolutionary and the other two are essentially
for further specialization and diversification (Stebbins macroevolutionary: (i) differential trait transition rates,
1974). These venerable ideas need further scrutiny in (ii)differentialextinctionrates,and(iii)differentialspeci- D
o
ordertodevelopaprogrammefortestingthevalidityof ation rates (Fig. 1). To illustrate the operation of these w
n
theircomponents. processes in more detail, consider a clade of plants lo
a
d
In more recent years, discussions about the types, where three-quarters of the species have flowers with e
d
causesandeffectsoffloralspecializationandpollination petals,eventhoughthebasalconditionisforflowersto fro
m
syndromeshavecometothefore.Atthecoreofmanyof lack petals. If petals are adaptive (sayattracting more h
theseargumentsliesuncertaintyaboutthefundamental pollinators,increasingreproductivesuccess),theremay ttp
s
conceptofplantfitnesstrade-offs,whereadaptationto be differential transitions between states (Fig. 1), such ://a
c
one type of pollinator incurs costs in terms of reduced that lineages with flowers lacking petals sometimes a
d
e
effectivenessofanothertype(Aigner2001,2004,2006). evolve them, but once evolved, they are rarely lost m
Isthisubiquitous,commonorrare?Consensus,ifthereis (i.e.lineageswithpetaliferousflowersalmostneverre- ic.o
u
any,seemstobethattrade-offsarefrequentlyweakor verttobeingapetalous).Thuspetalsareakeyinnovation p
.c
absent (see Castellanos et al. 2004; Muchhala 2007), inanadaptive(microevolutionary)sense:theyenhance om
althoughthereareprobablytoofewstudiesforconclu- reproductive success of individuals and populations, /a
o
b
sionstobedrawn. whichinturncausesfrequentmicroevolutionarytransi- p
la
BelowIaddresstheseissuesbydiscussingpollination tionstothestate.Ifwehaveenoughphylogeneticinfor- /a
andfloralspecializationinrelationtofitnesstrade-offs. mation, we may recognize the pattern this process rtic
le
I also review adaptive accuracy and floral precision as creates:parallelism(i.e.multipleoriginsofpetals).How- -a
b
theyrelatetomechanismsofreproductiveisolation,di- ever,multipletransitionstohavingpetalscouldalsobe stra
versificationandevolutionofphenotypicdisparity(mor- crypticifthetaxaarecloselyrelated,the phylogenetic ct/d
phologicaldiversity). treeispoorlyresolved,taxaaremissingorintermediate o
i/1
lineages have gone extinct. There might be only one 0
.1
Evolutionarysuccess:diversityandphenotypic origindetected,whenactuallyseveraltransitionshave 09
disparity occurred. 3/a
o
Evolutionarysuccessiscommonlymeasuredasthenum- Differencesinthenumberofpetaliferousandapetalous bp
la
berofspecies(richnessordiversity)inaclade,sometimes speciesinacladecanalsocomeaboutthroughdifferential /p
lu
in combination with the ecological/morphological vari- extinction.Strictlyspeakingthisisamacroevolutionary 0
0
ation (‘phenotypic disparity’) of those species (Hunter property,forexample,aswhenthebiological‘decksare 3/1
5
1998;Schluter2000).[Phenotypicdisparityisalsocalled cleared’ by astronomically induced mass extinctions 6
1
‘morphological’or‘phenotypicdiversity’,butIuse‘dispar- (e.g. by large-meteor impacts). However, if extinction 96
b
ity’heretofollowatraditionalreadywellestablishedin has occurred overextended periods (sometimes called y
g
the zoological literature (e.g. Wills et al. 1994; Foote the ‘background extinction’ rate), not in a single pulse, u
e
s
1997; Harmon et al. 2003; Hughes et al. 2013) and to there is a likely link to normal microevolutionary pro- t o
n
keepacleardistinctionfromspeciesdiversity.]Lineages cesses.Thusif petalsattractmorepollinators,resulting 2
0
withmanyextantspeciesareconsideredmoresuccessful in better pollination and lower rates of reproductive A
p
than ones with very few. Lineages exhibiting greater ril 2
phenotypicdisparity(phenotypicdiversity)areexpected 0
1
9
to be more successful because they may have greater
capacity for further diversification (although the data
supporting this expectation are few). The combination
of relatively rapid diversification with greatly increased
disparity (phenotypic diversity) is often referred to as
‘adaptive radiation’ (Simpson 1953; Schluter 2000). In
turn,we canassesstraits(character states) associated
Figure1. Causesofdifferencesinspeciesdiversityoflineageswith
withevolutionarysuccess,whicharecalled‘keyinnova- differentcharacterstates,here,forexample,bearingflowerswith
tions’, e.g. powered flight in insects, birds and bats, or, (petaliferous)andwithout(apetalous)petals.
2 AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014
Armbruster—Floralspecializationandangiospermdiversity
failure, lineages with petals would tend to experience ofpollinatorimportance(PI)is
lowerprobabilitiesofextinction.
Finally,ifpetalspromoteattractionofparticularkinds PI=V×A×S (2)
ofpollinators,thepresenceofpetalsmightincreasespe-
where V is the visitation rate per unit time, A is the
ciation rates by promoting pre-pollination reproductive
per-visit probability of contacting the anthers and S is
isolation from related taxa. This could come about in
the per-visit probability of contacting the stigmas
threeways:(i)attractingandrewardingasetofpollinator
(Armbruster1985,1988,1990).
speciesnotusedbyrelatedplantspecies,(ii)petalsenfor- D
cingspecializedhandling,promotingassociativelearning Freitas(2013)hascometoasimilarconclusionabout ow
n
orotherwiseenhancingconstancy(temporaryfloralspe- the confusion caused by these semantics. He recom- lo
a
mendscallingvisitationrate‘visitationintensity’andeffi- d
cialization by individual animals), or (iii) petals causing e
d
pollen placement and stigma contact in places on the ciency ‘efficacy’, but otherwise his recommendations fro
largelyagreewiththeabove. m
pollinatornotusedbyotherspecies.VerneGrant (1949, h
1971,1994a)classified(i)and(ii)asethologicalisolation ttp
and(iii)asmechanicalisolation. Floral isolation. Before evaluating the role of floral s://a
specializationindiversification,itisnecessarytodefine c
a
d
floral isolation precisely. Considerable confusion exists e
Semanticissues m
in the literature because the term has been used in at ic
.o
Pollinator importance, effectiveness, efficiency and least two ways (see Fig. 2): (i) floral isolation sensu u
p
abundance. Stebbins (1970, 1974) proposed the ‘most stricto (s.s.), which implies biologically significant .co
m
effectivepollinatorprinciple’whichstatesthat: reproductive isolation as a result of floral traits acting /a
o
on their own (i.e. floral isolation as a category of b
Sinceselectionisaquantitativeprocess,thecharacteristics p
oftheflowerwillbemoldedbythosepollinatorsthatvisit reproductive isolation; see Grant 1949, 1971, 1994a, b; la/a
itmost frequentlyandeffectivelyintheregionwhereitis reviewed in Kayand Sargent 2009); (ii) floral ‘isolation’ rtic
evolving. le
sensu lato (s.l.), where there is some segregation of -a
b
Althoughtheintentionofthisstatementisclearinthis pollenflow,i.e.moreintraspecificandlessinterspecific, s
tra
context,Stebbins’unfortunate useof‘effective’bothin without necessarily resulting in biologically significant c
t/d
thenameoftheprincipleandasacomponentofimport- reproductive isolation (e.g. Huang and Shi 2013; see o
i/1
ance in natural selection has led to confusion about the discussion in Kayand Sargent 2009). One problem 0
.1
which pollinators are expected to be driving selection. with this dichotomy is: what is meant by ‘biologically 0
9
3
Myinterpretation of whatStebbinsmeantinthis state- significant’,andcaniteverbe definedorassessed?For /a
o
mentcanbeexpressedbychangingoneword: the purpose of this review, I will treat ‘biologically b
p
‘...thecharacteristicsoftheflowerwillbemoldedbythose significant isolation’ to be isolation that generates la/p
pollinatorsthatvisititmostfrequentlyand[efficiently]...’ segregation of gene flow sufficient to allow, by itself, lu0
0
geneticdivergenceofthepopulationinresponsetodrift 3
(i.e.themosteffectivepollinators).[Asnotedbelow,we /1
5
6
should probably also insert ‘usually’ in this statement; 1
9
6
whenfitnesstrade-offsinpollinatoruseareabsent,the b
y
‘moulding’pollinatormaynotbethemosteffectiveone g
u
(Aigner2001).] es
ThusIrecommendwedefinepollinatoreffectiveness t o
n
as the product (or a similar function) of visitation rate 20
A
(frequency)andper-visitefficiency(measuredaspollen p
delivered,seedsproduced,offspringsired,etc.,pervisit; Figure2. Complexlinksbetweenfloralspecialization,floral‘isola- ril 2
0
seealsoFreitas2013).Forexample, tion’andcladespeciesdiversity/richness.Specializedflowersmay 19
increasethelikelihoodoffloralisolationinthestrictsenseand/or
pollinatoreffectiveness = visitationrate×efficiency (1) inthebroadsense.Increasedoccurrenceoffloralisolation,inthe
strictsense,mayincreasethespeciationrateandhencecladespe-
Earlier mycolleaguesand Ihaveused‘pollinatorim- cies richness and diversity. Alternatively, floral ‘isolation’, in the
portance’asalessambiguousterm,butconceptuallyre- broadsense,maydecreasetherateofextinctionandleadtoin-
creasesincladespeciesrichnessandtherebydiversity.Inturn,in-
latedtoeffectivenessasdefinedabove(Armbruster1985,
creased species diversity of clades may increase the number of
1988,1990;Armbrusteretal.2000;Fensteretal.2004).
clade members occurring in sympatry, therebyselecting for im-
Wereferredtothepollinatorwiththehighestimportance provementsinfloralisolationinthebroadsense,whichmaybeman-
scoreasthe‘principalpollinator’.Onepracticalestimator ifestedbyincreasedfloralspecialization.
AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014 3
Armbruster—Floralspecializationandangiospermdiversity
or weak selection. Thus narrow-sense floral isolation specialization/generalization’ sensu Ollerton et al.
acting by itself generates sufficient reproductive (2007) refers instead to the number of higher taxa
isolationtopreventorretardgenetichomogenizationof being pollinators (e.g. bees, birds, bats). This contrasts
populations. In contrast, broad-sense floral ‘isolation’ withwhatthesesameauthorscalled‘ecologicalspecial-
includes anything that reduces inter-morph mating ization/generalization’:thenumberofspeciesofpollina-
even bya few percentage points, and may or may not tors. ‘Ecological specialization’ sensu Ollerton et al.
have anydirect genetic consequences. Because I think (2007) differsfromtheuse byArmbrusteret al.(2000),
offloralisolationasatypeofreproductiveisolationand Fensteretal.(2004)andtheuseadoptedhere.] D
o
because reproductive isolation is commonly defined Ollertonetal.(2007)coinedtheterm‘phenotypicspe- w
n
as ‘the inability of a species to breed successfully cialization’offlowers,wherethemorphology,colourand/ loa
d
with related species’ (Merriam-Webster 2013), I prefer orfragranceofaflowerisspecialized,eventhough the ed
to use ‘floral isolation’ in the narrow sense. In place of current pollinators may not be especially restricted. fro
m
‘floral isolation s.l.’, I will usually refer directly to the Thusaphenotypicallyspecializedflowermayhaveeco- h
selectivemechanismsinvolvedinreducinginterspecific logicallygeneralized pollination (by multiple functional ttp
s
pollination (e.g. divergent adaptations to different groups).Thisunexpectedoutcomemayreflectaholdover ://a
c
pollinators, reinforcement of reproductive isolation or fromapriorhistoryofspecialization,compensatoryadap- ad
e
characterdisplacement).AlthoughIdonotrecommend tationsfordealingsuccessfullywithavarietyofpollina- m
abandoning the term ‘floral isolation’, I urge that we tors,asmaybe the caseforStylidiumspp. (Armbruster ic.o
u
etal.1994,2004,2009a,b;seebelow),orthelackoffit- p
alwaysexplaininwhatsenseweareusingit. .c
nesstrade-offs in adaptingto pollinatorsthat increase om
marginalfitness(Aigner2001,2004,2006).Fitnesstrade- /a
Floral Specialization, Fitness Trade-offs o
b
offsin thiscontext arewhen atrait’s positiveeffecton p
and Adaptive Accuracy la
pollination effectivenessof one pollinator (fitness) cre- /a
The concept of specialization has several components ates a negative effect on pollination effectiveness of rtic
le
andmeaningsasappliedtoflowers.Themanifoldnature one or more other pollinators. Aigner (2001, 2006) ex- -a
b
of this concepthascreatedconsiderableconfusion and ploredtheeffectoffitnesstrade-offsintheevolutionof stra
discussion(cf.Ollerton1996;Waseretal.1996;Johnson phenotypic specialization, pointing out that, in the ab- ct/d
andSteiner2000;Fensteretal.2004;Ollertonetal.2007). sence of steep fitness trade-offs, phenotypic speciali- o
i/1
Armbruster et al. (2000; see also Fenster et al. 2004) zation can evolve without restricting the number of 0
.1
pointed out that specialization can refer either to a pollinatortypes(ecologicalgeneralizationismaintained; 09
3
state(beingspecialized:‘ecologicalspecialization’)orto seethediscussioninthenextsection).Incontrast,inthe /a
o
aprocess(becomingmorespecialized:‘evolutionaryspe- presenceofsteeptrade-offs,phenotypicspecializationin bp
la
cialization’).Thus,aspeciesmaybelegitimatelyviewed responsetoselectionbyonepollinatorspeciesresultsin /p
lu
asunspecializedecologically,butspecializedevolutionar- fewerfunctionaltypesofpollinatorsthatcanbeutilized 0
0
ily,ifitismorespecializedthanitsancestors. (ecological and evolutionary specialization). Muchhala 3/1
5
Fundamentaltothedefinitionoffloralspecializationis etal.(2010)exploredtheroleofpollenfatesintheevo- 6
1
thequestionofwhatisbeingspecializedon.Classically, lution of floral specialization. Individual-based models 96
b
specializedpollinationhasreferredtothenumberofspe- indicatedthatmalefitnessdifferentialscandrivetheevo- y
g
ciesofanimalsthatpollinate theflowers,henceacon- lutionofecologicalandphenotypicspecializationevenin u
e
s
tinuous spectrum, from one species (specialized) to theabsenceoffitnesstrade-offs. t o
n
manyspecies(generalized).Morerecently,theconcept 2
ofspecializationvs.generalizationinpollinationhasfo- Fitnesstrade-offs 0 A
p
cusedonfunctionalgroupsofpollinators.Thistermwas Theabovestudiesunderscoretheimportanceofunder- ril 2
apparentlycoinedindependently(butwithsimilarmean- standing how often fitness trade-offs between floral 0
1
9
ing) by Corbet (1997—‘function group’), Johnson and adaptations to different pollinators occur, not least
Steiner (2000—‘function type’) and Fenster et al. because floralspecialization ispromoted bythe fitness
(2004—‘functional group’).Pollinator functional groups trade-offs between pollinators (e.g. Schemske and
areanimalsthatgeneratesimilarselectionpressureson Horvitz 1984; Wilson and Thomson 1996; Aigner 2001;
flowers, e.g. bees with similar tongue lengths, even Mayfield et al. 2001; cf. Muchhala et al. 2010). Aigner’s
thoughtheymaybelongtodifferentgeneraorfamilies own studies (2001, 2004, 2006) suggested that fitness
(JohnsonandSteiner2000;Fensteretal.2004).[Thisis trade-offswereabsentinpollinationofgeneralistDudleya
similar but not the same as what Ollerton et al. (2007) flowers by large bees, small bees and hummingbirds.
refer to by ‘functional specialization’. ‘Functional Aigner (2006) reviewed a number of studies that
4 AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014
Armbruster—Floralspecializationandangiospermdiversity
suggestedtrade-offsinfloraladaptationtopollinationby inSchluter2000;SvenssonandCalsbeek2012).Because
differentagents,butmostofthesestudieseitherfailedto thisapproachprovidesuncontrolledcomparativeresults
elucidate the functional basis of fitness trade-offs or ratherthancontrolledexperimentalones,itisnecessary
failedtoaccount for bothcomponentsof pollinatoref- tobemorecautiousininterpretation,beingalerttopos-
fectiveness(abundanceandefficiency),whichleavesun- sible confounding factors. Nevertheless, clear fitness
certaintyabouttheimportanceofthetrade-offsinthose trade-offs in Dalechampia (Euphorbiaceae) pollina-
systems. tion were documented using intra-population, inter-
AnelegantexperimentalstudywithPenstemon(Plan- population and inter-species comparisons to estimate D
o
taginaceae) showed no detectable fitness trade-offs theshapeoftheadaptivesurface.Theseplantshavebi- w
n
acrosstraits affecting hummingbird vs. bee pollination laterally symmetrical blossoms (pseudanthial inflores- lo
a
d
(Castellanos et al. 2004). Another experimental study, cences)withpollinationbyresin-collectingbees(which e
d
which did detect clear trade-offs, is Muchhala’s (2007) use the resin for nest construction) of arange of sizes. fro
m
studyofhummingbirdandbat‘pollination’.Thisinvolved Analysesshowedthatadaptationtopollinationbylarge h
artificialflowersofdifferentwidths,capturingthemorph- resin-collecting bees (Apidae: Eulaema, Eufriesea) re- ttp
s
ology of two species of Burmeistera (Campanulaceae), ducedorprecluded,respectively,pollinationbymedium- ://a
c
one primarily hummingbird pollinated (narrow floral sized resin-collecting bees (Apidae: Euglossa) and a
d
e
tube)andtheotherprimarilybatpollinated(widefloral smallresin-collectingbees(Megachilidae:Hypanthidium; m
tube).Hummingbirds werebetterat transferringpollen Armbruster1985,1988,1990,2006;Hansenetal.2000). ic.o
u
betweennarrow-tube‘flowers’,andbatsbetterattrans- Thistrade-offoperatedasaninteractionbetween(i)at- p
.c
ferringpollenbetweenwide-tubed‘flowers’.Importantly, tractionandvisitationrate,asdeterminedbytheamount om
intermediate-widthtubes(generalists)performedworse ofresinreward,and(2)pollinatorefficiency,measuredas /a
o
b
than the narrow tubes with hummingbirds and worse theproductoftheratesofbeecontactwithstigmasand p
la
thanthebroadtubeswithbats(andhadlowest‘pollination’ withanthers.Thisinteractioncreatesapositive-diagonal, /a
overall),demonstratingacleartrade-offfavouringtwospe- adaptiveridge(in3-traitspace),whichisalsoanaxisof rtic
le
cializedphenotypesoveroneintermediategeneralist. specialization (attraction of and pollination by small -a
b
Temelesetal.(2009)describedanintriguingsystemin- bees, medium-sized bees or large bees). Off-diagonal stra
volving sexually dimorphic purple-throated carib hum- traitcombinationshaveeithermoregeneralizedpollin- ct/d
mingbirds(Eulampisjugularis)exertingselectiononthe ationwithlowerfitness(attractionandpollinationbyall o
i/1
shapeofHeliconia(Heliconiaceae)flowers.Usingartificial bee sizes with wasteful reward investment and loss of 0
.1
flowers, they discovered trade-offs in handling time, pollen to other sympatric Dalechampia species) or ex- 09
3
where females, which have long, curved bills, handled tremely low pollination rates (attraction of only small /a
o
longerflowers(ofallcurvatures)morequicklyandeffect- bees when stigmas are contacted only by large bees; bp
la
ively,obtainingthedeepernectar,thanthemales,which Fig. 3; Armbruster 1988, 1990, 2006). All populations /p
lu
haveshort,straightbills.Inturn,maleshadshorterhand- andspecieswereobservedtooccupythepredictedadap- 0
0
ling timesthan femalesonartificialflowers withshort, tive ridge. This ridge is an allometric trajectory, so it is 3/1
5
straightcorollas(butonlywhenhovering).Althoughthe possible that the relationship is pleiotropic rather than 6
1
measuredtrade-offswereexperiencedbythepollinator, created by a fitness trade-off, although phenotypic 96
b
theysuggestedanindirectplantfitnesstrade-off,where (Armbruster 1991) and quantitative-genetic (Hansen y
g
bothbirdsandplantsshouldspecializeontheappropri- etal.2003a,b)datasuggestthatthisisveryunlikely. u
e
s
atemorphs,withselectionagainstgeneralists(Temeles Anothercomparativestudysystemexhibitingbilaterally t o
n
etal.2013). symmetrical flowers and apparent fitness trade-offs is 2
0
Schemske and Bradshaw (1999) and Bradshaw and the genus Collinsia (Plantaginaceae). These annuals A
p
Schemske(2003)foundthatvariationinflowercolourin haveflowersresemblingpeaflowersinhavingstamens ril 2
hybrid Mimulus created atrade-off, affecting visitation andstyleenclosedinakeel-likefoldofthelowercorolla 0
1
9
ratesofbeesandhummingbirdsinoppositedirections. lobe(seeKaliszetal.1999).Thekeelisdepressedwhen
However, variation in nectar volume and petal surface alightingbeesareofsufficientmass(inpassivedepres-
areadidnotcreatetrade-offs,havingsignificanteffects sion)orstrength(inactivedepression).Withdepression
on onlyone of the twopollinator types(Schemskeand ofthekeel,thestigmacontacts,and/orpollenisdepos-
Bradshaw1999). ited on, the underside of the bee (Fig. 4; Armbruster
There is also an older literature addressing fitness etal.2002,2004,2009a).Variationinflowersizeandped-
trade-offs in pollination using natural variation among uncle(floralstem)strengthcreatescontinuousvariation
populationsandspecies.Trade-offs,ifany,aredisplayed in‘optimal’pollinatorsize.Large-floweredspeciesattract
intheshapesofestimatedadaptivesurfaces(seereviews largebees(Apidae:Bombus,Anthophora,etc.)andhave
AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014 5
Armbruster—Floralspecializationandangiospermdiversity
D
o
w
n
lo
a
d
e
d
fro
m
h
ttp
s
://a
c
a
d
e
m
ic
.o
u
Figure4. FlowerofCollinsiasparsiflorawithpollinatingmaleEucera p
(Tetralonia)bee(Apidae:Anthophorinae).Thekeelofthelowerlipis .co
m
partiallydepressed,withthefertilepartcontactingtheundersideof /a
thethorax. ob
p
la
/a
Figure3. Adaptive‘ridge’(aseriesofconcentriccigar-shapedvo- an experiment, one cannot rule out that the apparent rtic
lumes)inthree-traitspace,capturingfitnesstrade-offsinDalecham- le
pia spp. with resin rewards. Adaptation to small-bee pollinators trade-offcouldbeeliminatedbyselectionforgeneralized -a
b
precludesvisitationbylargebees,whileadaptationtolarge-beepol- pollination,butitseemsunlikely. stra
lbinluaet,otrhseprheigclhuedretshsemfiatnlle-bseseinptohllaintavtoolrusm.Teh.eOfdfa-drkiaegrotnhaelsvhoaludmeeosf thaPetrturasadleo-offpfsubsleisehmedmsoturedileikseslyugtogeosctscutrheinhbyiplaottehreaslliys ct/do
(clear)experiencelowestfitness.Region1isavolumeoflowfitness i/1
symmetrical (zygomorphic) flowers than radially sym- 0
becauseonlysmallbeesareattracted,butonlylargebeescontact .1
metric flowers. However, a notable exception to this 0
stigmasandanthers.Region2isavolumeoflowfitnessbecause 9
3
resincostsexceedpollinationbenefits,and/orgreaterinterspecific trend is found in the plant genus Stylidium (‘trigger- /a
o
pollinationoccurs.Region3isavolumeoflowfitnessbecause,al- plants’, Stylidiaceae). These Australasian herbs and bp
thoughthesmallbeesattractedtouchthestigmas,theydonot shrubs have phenotypically highly specialized, protan- la/p
carrypollenbecausetheydonotcontacttheanthers. drousflowersthatarezygomorphicandbearnectarina lu0
0
tube or spur. The column (gynostemium) is formed by 3/1
strongpedunclestosupporttheweight.Theseflowersare fused pistillate and staminate tissues and is motile, 56
1
alsovisitedbysmallerbees(Megachilidae:Osmiaspp.,es- ‘explosively’depositingpollenon,orretrievingitfrom,the 96
peciallymales;variousHalictidae),butthesebeesaretoo pollinatorin10–15ms(Fig.5;Findlay1978;Armbruster by
g
smalltodepressthekeel,andtheyobtainnectar(nectar etal.1994,2004,2009a).Theflowersareecologicalgen- u
e
s
thieves)orgleanstraypollenwithoutcontactinganthers eralists, attracting alarge numberof speciesinseveral t o
or stigmas. Small-flowered species of Collinsia, in con- functiongroupsofpollinators(smallbees,largebees,syr- n 2
0
trast,donotusuallyattractlargebees,bothbecauseof phid flies, and small-, medium- and large-bodied bee A
p
less nectar (Heinrich and Raven 1972) and because if flies). All functional groups are similarly effective ril 2
largebeesvisitsmall-floweredspeciesthepedunclescol- pollinatorsacrossarangeofflowersizes.Thefitnesscon- 0
1
lapseundertheirweightandthebeesaredumpedonto tributionsofpollinatorsareadditive;therearenodetect- 9
theground(anexperiencethebeesseemtoavoid).The able trade-offsover the range of floral visitors in these
corolla of small flowers is lightlyspring-loaded so that functional groups. This is because, except for the ex-
smallbeescandepressthekeelandactasgoodpollina- tremes, the flowers do not experience morphological,
tors.Theallometryoffloralsizeandaccompanying‘en- fit-relatedtrade-offs,wherethesizeof theflowermust
gineering’ creates an apparent trade-off, where large matchexactlythesizeandshapeofthepollinatorforpol-
flowers can be pollinated by large bees but not small lentobepickedupanddeposited,asdescribedabove.In-
ones,andsmallflowerscanbepollinatedbysmallbees stead the motile column behaviourally ‘adapts’ to size
butareseldomvisitedbylargeones.Intheabsenceof andshapeofthediversepollinators.Pollenisdeposited
6 AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014
Armbruster—Floralspecializationandangiospermdiversity
trade-offsincertainkindsofflowers,e.g.mostzygomor-
phic,andnotothers,e.g.manyactinomorphic,coulddrive
evolutiontowardsecologicalspecializationandperhaps
greater diversification in certain groups (e.g. Sargent
2004). Indeed, phylogenetic-comparative analyses of
theevolutionanddiversificationconsequencesoffitness
trade-offsacrosspollinatortypesshouldbeafruitfulline
ofinvestigation. D
o
w
n
Conflicting selection generated by abiotic factors and lo
a
multi-species interactions with flowers. It is now well d
e
d
recognized that plants interact with a diversity of fro
mutualists and antagonists, from pollinators and m
h
Figure5. Stylidiumdichotomumflowerinfemalephaseretrieving defendingantstonectarrobbers,florivores,folivoresand ttp
pobotllaeinninfrgomnecLteairo.proctus sp. which has sprung the column while p(Sattrhaougssenasn,dinIrwbionth20e0c4o;lMogcCicaalllaannddIrewvoinlu2t0io0n6a;rSytrtaiumses s://ac
a
d
andWhittall2006;Irwinetal.2010).Forexample,while e
m
and stigmas make contact in the same location on a advertisementtraitsincreasetheapparencyofflowersto ic.o
givenpollinatorspecies.However,anther/stigmacontact pollinators, raising fitness, they may also increase the up
.c
isindifferentlocationsondifferentpollinatorspecies,but apparencytoenemies suchasnectarrobbers,florivores o
m
consistently so: e.g. Stylidium lineatum places and re- and seed predators, lowering fitness. Thus floral traits /a
o
trievespollenatthetipoftheabdomenofmedium-sized may commonly be subject to conflicting selection bp
la
beeflies,thetopofthethoraxoflargebeefliesandthe mediated by mutualists and antagonists, resulting in /a
front of the head of large anthophorid bees (W. S. complex trade-offs. Depending on the shape of the rtic
le
Armbruster,unpubl.res.).Thusthecomplex,specialized fitnessresponsestotheconflictingrelationships,thenet -a
b
Stylidium floralmorphologyandtriggerbehaviour work result may often be stabilizing selection. The role of stra
equallywellwithavarietyofsizesandshapesofpollina- multiple species in generating stabilizing selection may ct/d
tors.Infacttheflowercouldbedescribedasphenotypic- helpinexplainingwhyphenotypicselectionstudiesthat o
i/1
allyspecializedtobeanexcellentecologicalgeneralist. addressonlyoneinteraction, asisoftenthecase, more 0
.1
Therearegoodreasonsalsotothinkthatmostopen, oftendocumentdirectionalselectionthantheotherwise 09
3
actinomorphic(radial)flowers(e.g.Dudleya)andcapitu- expectedstabilizingselection. /a
o
lae(e.g.mostAsteraceae)usuallylackfitnesstrade-offs Numerous examplesof conflicting selection on floral bp
across a broad range of pollinator functional groups. traits have been published, and several papers review la/p
However,thisisnotalwaysthecase.Thereareapparent the topic thoroughly (e.g. Brody 1997; Cariveau et al. lu0
0
trade-offs in rates of contact with stigmas for actino- 2004; Strauss and Irwin 2004; McCall and Irwin 2006; 3/1
morphic flowers with ‘apertures’ of some sort, where StraussandWhittall2006;Irwinetal.2010).Oneofthe 56
1
theapertureinteractswithpollinatorsize.Forexample, earliest well-documented examples is the observation 96
in some Linum(Linaceae) and Parnassia(Celastraceae/ of conflicting selection on floral fragrance and flower by
g
Parnassiaceae)speciesandinmostPassiflora(Passiflora- shape of Polemoniumviscosum generated byants and u
e
s
ceae),fliesandbeesthataretoolargetofitthroughthe bumble bees in the subalpine Colorado (Galen 1999; t o
gapformedbypetalsandfertilepartsareexcludedfrom Galenetal.1987,2011).Averyrecentexampleisthede- n 2
0
reachingnectarand arerarelygood pollinators. Exces- tectionofconflictingselectiononthesizeoffloralbracts A
p
sivelysmallfliesandbeeshaveaccesstothenectarbut ofDalechampiascandensinMexico,withpositiveselec- ril 2
usuallyslippasttheanthersandstigmaswithoutmaking tiongeneratedbypollinatingbeesandnegativeselection 0
1
contact,thusfailingtopickupordepositpollen(highvis- generatedbycurculionidseedpredators(Pe´rez-Barrales 9
itation,lowpollinationefficiency;Armbrusteretal.2006, etal.2013).
2009a,2014a;Benevidesetal.2013). Additional complexity in floral evolution may result
Ideally,alloftheabovecomparativesystemsshouldbe from conflictingselection generated by pollinatorsand
testedexperimentallyusingfactorialanalyseswithdiffer- abiotic factors.Forexample,pollinators oftenselectfor
entspeciesofpollinatorsanddifferentfloralphenotypes largercorollasize,butsuchincreasesexertalargecost
(Wilsonand Thomson1996;Muchhala2007).However, intermsofwaterlossindryenvironments(Galen2000;
Ithinkitissafetoaccept,atleastprovisionally,theresults Lambrecht and Dawson 2007). Selection to speed up
ofthesecomparativeanalyses. Theexistenceof fitness thelifecycleinhighlyseasonalenvironmentsmayresult
AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014 7
Armbruster—Floralspecializationandangiospermdiversity
inselectionagainstlargeflowers,inconflictwithselec- andredistributionofpollenonthepollinatorandeffects
tiongeneratedbypollinators(RunionsandGeber2000; of other ecological factors (e.g. other pollinators, flori-
Mazeretal.2004;Lambrecht2013;butseealsoMoeller vores,predators).Therealizedprecisionofpollinationis
andGeber2005). nearly always lower than the fundamental precision,
andthereforethisasymmetryalsoholdsforaccuracies.
Adaptiveaccuracyofflowers
Anotherapproachtoassessingfitnesstrade-offsandpos- Mechanisms of Diversification
sibleconnectionsbetweenfloralspecializationandflower- D
o
ing-plantdiversificationinvolvesadaptiveaccuracytheory. From the overview presented in the Introduction, it is w
n
This approach, which can be used in this context to clearthatflowersmayinfluencediversificationinseveral loa
quantifypollinationaccuracy,isalsousefulforassessing ways,involvingbothadaptive(traittransitions,reduced ded
theabilityoftheflowersofsympatricspeciestogenerate extinctionrates,adaptive/ecologicalspeciation)andnon- fro
adaptive processes (e.g. non-adaptive speciation). Be- m
segregatedpollenflowandmaintainreproductiveisola- h
tion(ornot). causetheinfluenceofadaptiveprocesseson‘ecological’ ttp
s
Adaptive inaccuracy estimates the phenotypic load and ‘adaptive’ speciation has been reviewed recently ://a
(maladaptation)thatresultsfromphenotypicdeparture elsewhere(Dieckmannetal.2004;Johnson2006,2010; cad
from the optimum in a population. At the level of the Nosil2012;vanderNietandJohnson2012),itisnotcov- em
population,thereareatleastthreecomponents,which ered in detail here. However, it should be remembered ic.o
are additive (Armbruster et al. 2004, 2009a; Hansen thattheeffectonplantspeciationofadaptationtopolli- up.c
et al. 2006; Pe´labon et al. 2012): (i) optimality of the natorsispotentiallyofgreatimportance(Johnson2006, om
mean, which is how far the mean of events departs 2010;vanderNietandJohnson2012).Inbothallopatry /ao
from the optimum (¼‘maladaptive bias’), (ii) the vari- and sympatry, adaptive divergence of floral traits can bp
la
ance,whichishowmuchindividualsvaryfromthemean leadindirectly totheestablishmentof barrierstointer- /a
(¼‘adaptive imprecision’), and (iii) the variance in the breeding.Additionally,adaptivereinforcementofrepro- rticle
optimum. By extrapolation from measurement theory ductiveisolation(‘Wallaceeffect’;Grant1966;Silvertown -a
b
(Armbruster et al. 2004; Pe´labon et al. 2012), these et al. 2005) and reproductive character displacement stra
(Grant 1972) may further promote speciation rates and c
threecomponentssumtotheadaptiveinaccuracyas t/d
hencediversification.Incontrast,non-adaptivespeciation, o
i/1
adaptiveinaccuracy=(traitmean − optimumvalue)2 evenifrare,isofconceptualimportancebecauseitpoten- 0
.1
+trait variance+optimumvariance tiallydecouplesspecies-levelselection(Stanley1975)from 09
3
(3) microevolution(Gould2002).Thecommonestformofnon- /ao
adaptivespeciation(inthesenseofthebiological-species b
p
Although phenotypic selection only detects relative definition)inplantsisprobablypolyploidy.Non-adaptive la/p
overalladaptiveinaccuracyofflowers (asacomponent (‘instantaneous’)speciationhasalsobeensuggestedfor lu0
0
ofreproductivefitness;Armbrusteretal.2004,2009a,b), the origins of fragrance ‘races’ and new species in 3/1
genetic response to phenotypic selection may occur male-euglossine-pollinatedorchidsandsexuallydeceptive 56
1
through reducing the maladaptive bias (less departure orchids(Dressler1968;CozzolinoandWidmer2005). 96
b
fromtheoptimum),decreasing(orincreasing)theadap- y
tiveimprecision, decreasing(orincreasing) thevariance Specializationandcladesuccess gu
e
s
intheoptimumorsomecombinationofallthree. Featuresthatpromotespecializationarecommonlyinter- t o
n
Therearetwonewaspectsofadaptiveaccuracythat pretedaskeyinnovations,althoughtherearereasonsto 2
0
needtobeconsideredinthecontextofpollination:(i)fun- be cautious in making this assumption. For example, A
p
damentalaccuracyandprecision,and(ii)realizedaccur- dependenceonasingleobligatemutualistmaygreatly ril 2
acy and precision (terms were derived by analogy to increasetheriskofextinction(Waseretal.1996).Never- 0
1
9
ecological niche concepts; see also Armbruster et al. theless, the relationship between specialization and
2014b).Fundamentalpollinationaccuracyrelatestomea- clade ‘success’ has fascinated biologists since Darwin.
surements of optimality, precision and accuracy taken Botanists and zoologists have often thought about the
fromthefloweritself.Thisisonlyapredictoroftheactual relationshipbetweenthesetwopropertiessomewhatdif-
accuracyinplayecologically,therealizedpollinationac- ferently.Zoologistshavelargelyconsideredspecialization
curacy.Thelatterthenreferstotheinteractionof floral tobeadaptive,leadingtoadaptiveevolutionandevolu-
parts with the pollinator itself. It reflectsthe effects of tionarysuccess(highertransitionratesandlowerextinc-
thepollinators’behaviourininteractingwiththeflower tion rates; e.g. Schmidt-Kittler 2002; Ferna´ndez-Mar´ın
(e.g.variationinapproachandlanding),thedistribution et al. 2004; Litman et al. 2011; Eastman et al. 2013).
8 AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014
Armbruster—Floralspecializationandangiospermdiversity
Surprisingly, evolutionary botanists, in contrast, have inbreedingdepressionandmightpromotethepersistence
probablywrittenmore,atleastimplicitly in earlylitera- ofmixedmatingsystems(ArmbrusterandRogers2004;
ture,aboutnon-adaptiveprocessessuchasnon-adaptive Goodwillieetal.2005;LankinenandArmbruster2007;cf.
speciation,where,forexample,use of differentpollina- Igic and Busch 2013). The structures and secretions of
torsisthoughttoleadincidentallytoreproductiveisola- angiospermflowersalsopromoteusinganimalsforpollen
tionandtherebyincreasespeciationrates(Grant1949, andseeddispersal;thismayhaveallowedpopulationsto
1971, 1994a; Hodges and Arnold 1995; Hodges 1997; bemoredispersedandachievetargetedcolonizationoffa-
Sargent 2004; but see Stebbins 1974; Johnson 2006). vourablemicroenvironments(Stebbins1974;Regal1977; D
o
(Ecological speciation isincluded in this argument, but CrepetandNiklas2009).Allofthesefeaturesshouldlead w
n
it is less clear how adaptive specialization on different togreaterpopulationpersistenceandhencelowerextinc- lo
a
d
pollinatorsaffectsspeciationrates.) tionrates. e
d
Therole of floralspecializationin reducingextinction Anotheradvantageofangiospermflowersisthatthey fro
m
rates is rarely discussed, although Hodges and Arnold are modular units comprising many parts of differing h
(1995)mention‘increasedreproductivesuccess’asapos- degrees of integration. As modules, theycan maintain ttp
s
sible outcome of floral specialization. Research on the somedegreeofphenotypicindependencefromvariation ://a
c
roleofplantphysiologyandleafandstemanatomyand intherestof theplant,whichis adaptivein thefaceof a
d
e
function in evolutionary success also emphasizes the pollinator-mediated stabilizingselection for flower size m
adaptivenatureofspecialization(andimplicitlyreduced and shape (Berg 1960; Armbruster et al. 1999, 2004; ic.o
u
extinction; Gianoli 2004; Klak et al. 2004; Bakker et al. Hansen et al. 2007; Pe´labon et al. 2011; Murren 2012). p
.c
2005; Donoghue 2005; Guzman et al. 2009; Givnish Floral partsthemselves rangefromnearly independent om
2010). Although Johnson and colleagues (Johnson to highly integrated statistically (Connerand Via 1993; /a
o
b
2006, 2010; van der Niet et al. 2006; van der Niet and ConnerandSterling1995,1996;Armbrusteretal.1999, p
la
Johnson2012)haveemphasizedtheroleofadaptation 2004; Herrera 2001; Herrera et al. 2002; Anderson and /a
topollinatorsinbothallopatricandsympatricdivergence, Busch 2006; Hansen et al. 2007; Ordano et al. 2008; rtic
le
itislargelyinthecontextofspeciationratherthanrepro- Pe´labonetal.2011;Alcantaraetal.2013)orstructural- -a
b
ductivesuccessorpopulationviability. ly/developmentally (e.g. Armbrusteret al. 1994, 2004). stra
Itseemsclearthatfloralspecializationisoftenasso- Thisvariationindegreeofintegrationallowstremendous ct/d
ciatedwithcladesuccess(speciesrichness;Hodgesand adaptabilityinresponsetoselectionbydifferentpollina- o
i/1
Arnold 1995; Hodges 1997; Sargent 2004; Kay and tors.Forexample,ifsepalsareunderdifferentselection 0
.1
Sargent2009).However,itislessclearwhatcausesthis than petals, their quasi-independence allows different 09
3
association(seebelow;ArmbrusterandMuchhala2009). evolutionary responses (e.g. Armbruster et al. 1999). /a
o
Ifstylesandstamens,forexample,areselectedtobeof bp
Reducedextinction the same length (integration, in the face of variation), la/p
lu
Asalreadynoted,itiscommonlysuggestedthatflowering theycandosoeventhoughotherfloraltraitsexperience 0
0
plantsaresuccessfulandspeciesrichbecausereproduction differentselectivepressures(ConnerandVia1993;Conner 3/1
5
bymeansofflowersandfruitsismoreeffectiveoverallthan and Sterling 1995, 1996). Numerous semi-independent 6
1
bymeansofstrobili (e.g.Stebbins1974).Indeed,typical floralpartsalsoallowtheevolutionofadiversityofcom- 96
b
angiosperm flowers provide numerous potential advan- plexinteractionswithpollinators,and,infruit,seeddis- y
g
tagesovergymnospermstrobili.Theseincludemorerapid persers(Stebbins1974). u
e
s
development,whichmayhavebeenimportantincoloniz- Theaboveargumentsimply reduced extinction rates t o
n
ingandreproducingincomparativelyshort-livedorhighly for floweringplants compared with gymnosperms. The 2
0
seasonalhabitats.Flowersareusuallysmallerthanovulate rapidityof floraldevelopmentpresumablyalsoenabled A
p
strobili,whichallowsgreaterflexibilityinreproductivein- themtooccupynewenvironments,suchashighlysea- ril 2
vestment.Additionally,mostflowersarehermaphroditic, sonal and successional habitats (including post-fire 0
1
9
leading to efficiencies in pollination by animals, as well sites) requiring rapid growth and quick reproduction.
as potential reproductive assurance by autonomous Suchhabitatswerethoughttohavebecomemoreabun-
self-pollinationintheeventofpollinatorfailure.Anotherin- dantduringthe earlyand mid-Cretaceous,whenmuch
novation is that flowers provide an arena for extended angiosperm evolution was occurring (Axelrod 1970;
pollen-tubecompetition,whichmaypromoteoffspringfit- RavenandAxelrod1974;Stebbins1974;LamontandHe
ness by choice of superior sporophytic fathers (Mulcahy 2012). Flower structure and complexity as described
1979;SkogsmyrandLankinen2002;PannellandLabouche abovesuggestfurtherthatfloweringplantshadthepo-
2013).Pollencompetitionmayalsoscreenoutgenetically tential to radiate by use of different pollinators and
inferior male gametophytes, which potentially reduces seeddispersers(seeEvolutionoffloraldisparity,below).
AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014 9
Armbruster—Floralspecializationandangiospermdiversity
Theabovefeaturesleadtopotentiallyrapidandlabile basedonchemicalexploitationofoneorafewpollinator
evolutionary response of flowersto divergent selective species,whereaspollinationinfood-deceptiveorchidsis
pressures. Thisallows for increasingfloral disparity be- less specialized,attracting arange of pollinators much
tween species in sympatryand speciesin allopatry but as do food-reward flowers. Interestingly, post-mating
later in secondary sympatry. This capacity to diverge isolation has evolved in a clock-like manner, whereas
andspecializemaythusalsoreduceextinctionratesbe- pre-matingbarriers have not,supportingtheideathat,
cause itallowsthecompatible packingofmorespecies for angiosperms with food-deception and food-reward
(withnarrowerpollinationniches)intocommunities(i.e. pollinationsystems,speciationcommonlyoccursthrough D
o
with minimal reproductive costs incurred by sharing gradual divergence in allopatry (Cozzolino et al. 2005; w
n
pollinators). CozzolinoandScopece2008). lo
a
d
Anotherformofethologicalisolationoperatesthrough e
d
Increasedspeciationrates flower constancy, the tendency of individuals of some fro
m
A classicalexplanationfor high angiospermdiversityis speciesof animalstobetemporarilyfaithfultoasingle h
thatspecializedflower–pollinatorrelationshipsincrease flower species or morph (Grant 1950; Waser 1986). ttp
s
speciationrates.Thus,inadditiontoreducingextinction Thereareseveralpossiblereasonsthatanimals(mostly ://a
c
ratesandincreasingtheopportunityfortheevolutionof bees) mayadopt constancyas aforaging strategy, but a
d
e
disparity(seebelow),flowerswiththerightcombination the consensus is that it is a way to reduce handling m
of traits may have contributed to increased speciation time and possiblysearchefficiency.It canbe expected ic.o
u
rates in the angiosperms. Arguments and evidence for that floral features that increase a bee’s learning time p
.c
this relationship come from three sources: (i) classical for handling will promote greater constancy, although om
floral-isolation models, (ii) phylogenetic-comparative supporting data are sparse and weak (Chittka et al. /a
o
b
analyses,and(iii)ecologicalgeneticexperiments. 1999;Armbrusteretal. 2014b).Ifthisisthecase,how- p
la
ever,itcouldresultinhigherspeciationratesincomplex /a
Classical floral isolation model. As noted above, flowers and hence explain greater clade diversity (e.g. rtic
Grant (1949, 1971, 1994a) recognized the potential Sargent 2004; Kay and Sargent 2009). However, con- le-a
b
isimspoeplacoitraitntaigonncmereacothfeascnetihsrtmraoisun,gshkpineedcsitsfiacboalfilslyflhomtwherenorutsgoihfnpdirinfefc-erzeryeagnsocinteigcs sibsteoaclnaactuyisoeinsiutbneisltiwrkaeerleyentfooirnbacenipayiesanonltiemsmpaelectcoiheabseninipsmesyrfmoefcprtealyptrcryoo.dnTushtcaitsinvites. stract/do
in pollination ecology (floral isolation ss.). Complex Forexample,bumble bees, which are often highlycon- i/10
.1
flowers may attract only certain species of pollinators, stant,stillmakeoccasional(tonumerous)interspecific- 09
which could lead to floral isolation from related flower transitions (Heinrich 1976). Euglossine bees can 3/a
o
speciesattractingother pollinatorspecies.Thisformof be inconstant when flower handling is similar across bp
ethological isolation is based on traditional ideas of plantspecies(e.g.ArmbrusterandHerzig1984).Indeed la/p
specialization in flower–pollinator relationships, as Chittka et al. (1999) state: ‘...there is good evidence lu0
0
captured in older syndrome literature (see Faegri and againstthenotionthatpollinatorconstancyisinvolved 3/1
van der Pijl 1979). Some relationships between plants inspeciationormaintenanceofplantspeciesintegrity’. 56
1
and their pollinators are sufficiently specialized that Nevertheless, there are reasons to expect that plants 96
ethological isolation may influence speciation and will have evolved constancy-promoting floral features, by
g
reinforcement (e.g. in sexually deceptive orchids and becausetheseincreasereproductivefitness(dispersing u
e
s
plants pollinated by male-euglossine bees; Dressler more pollen to conspecific stigma and receiving more t o
1968; Cozzolino and Widmer 2005; Pansarin and do conspecificpollen),eventhoughtheserarelyplayarole n 2
0
Amaral2009;butseeArmbrusteretal.1992),butthisis inreproductiveisolation.Instead,becausefloralfeatures A
p
almost certainly the exception not the rule in increasingconstancy probablyplayarolein enhancing ril 2
angiosperms (Waser 1998, 2001; Armbruster and reproductivesuccess,theymayhaveincreaseddiversifi- 0
1
9
Muchhala2009). cationratesbyreducingextinctionrates(seeabove).
Someofthemostintriguingdataonethologicalisola- Certain floral traits may increase speciation rates
tioninorchidscomefromcomparisonsoffood-deceptive through enhancement of mechanical isolation (Grant
and sexually deceptive orchids (Scopece et al. 2007; 1949,1971,1994a),wherepollinatorsarerestrictedtoa
CozzolinoandScopece2008).Generally,sexuallydecep- subsetofvisitorsbythespecializedfitofflowersto‘pre-
tiveorchidshavestrongpre-matingisolationandweak ferred’pollinators,orwhereflowersplacepolleninaspe-
post-matingbarriers,whilefood-deceptiveorchidshave cific placeonthepollinator (withstigmacontactinthe
strongpost-matingisolation andweakpre-matingbar- same location) not used byother species.Earlystudies
riers. Sexual deception reflects unusual specialization of orchid speciation illustrate this concept nicely.
10 AoBPLANTS www.aobplants.oxfordjournals.org &TheAuthors2014