Recei ed: 8 May 2023
|
Accep ed: 11 May 2023
DOI: 10.1002/ajb2.16200
SPECIAL ISSUE ARTICLE
Pollen as he link be ween flo al pheno ype and fi ness
Øys ein H. Opedal
1
|Rocío Pé ez‐Ba ales
2
|Vinícius L. G. B i o
3
|
Na han Muchhala
4
|Miquel Capó
5
|Agnes Dellinge
6
1
Depa men o Biology, Lund Uni e si y,
Söl ega an 37, Lund 22362, Sweden
2
Bo any Depa men , Uni e si y o G anada,
G anada 18071, Spain
3
Ins i u o de Biologia, Uni e sidade Fede al de
Ube lândia, Ube lândia 38405‐315, B azil
4
Depa men o Biology, Uni e si y o Missou i a
Sain Louis, Sain Louis, MO, USA
5
Depa amen o de Sis emas y Recu sos Na u ales,
Uni e sidad Poli écnica de Mad id, Mad id, Spain
6
Depa men o Bo any and Biodi e si y Resea ch,
Uni e si y o Vienna, Vienna, Aus ia
Co espondence
Øys ein H. Opedal, Depa men o Biology, Lund
Uni e si y, Söl ega an 37, Lund 22362, Sweden.
Email: [email p o ec ed]
Abs ac
Pollen plays a key ole in plan ep oduc i e biology. Despi e he long his o y o esea ch
on pollen and pollina ion, ecen ad ances in pollen‐ acking me hods and s a is ical
app oaches o linking plan pheno ype, pollina ion pe o mance, and ep oduc i e fi ness
yield a s eady flow o exci ing new insigh s. In his in oduc ion o he Special Issue
“Pollen as he Link Be ween Pheno ype and Fi ness,”we s a by desc ibing a gene al
concep ual model linking unc ional classes o flo al pheno ypic ai s o pollina ion‐
ela ed pe o mance me ics and ep oduc i e fi ness. We use his model as a amewo k
o syn hesizing he ele an li e a u e, highligh ing he s udies included in he Special
Issue, and iden i ying gaps in ou unde s anding and oppo uni ies o u he
de elopmen o he field. The pape s ha ollow in his Special Issue p o ide new
insigh s in o he ela ionships be ween pollen p oduc ion, p esen a ion, flowe
mo phology, and pollina ion pe o mance (e.g., pollen deposi ion on o s igmas), he
ole o pollina o s in pollen ans e , and he consequences o he e ospecific pollen
deposi ion. Se e al o he s udies demons a e exci ing expe imen al and analy ical
app oaches ha should pa e he way o con inued wo k add essing he in iguing ole o
pollen in linking plan pheno ypes o ep oduc i e fi ness.
KEYWORDS
fi ness unc ion, flowe –pollina o fi , he e ospecific pollen ans e , pa h analysis, plan –pollina o
in e ac ions, pollen pe o mance, pollen p esen a ion, pollen p oduc ion, pollen ans e , pollina o ‐
media ed selec ion
Pollen plays a key ole in plan ep oduc i e biology
and is s udied in a ange o fields including cell and
molecula biology (Bedinge , 1992), biochemis y (S anley
and Linskens, 1974), ecology (Olle on, 2021), sys ema ic
biology (Ca dinal‐McTeague and Gillespie, 2016), and
e olu iona y bo any (Williams and Maze , 2016). As male
game ophy es, pollen sha e some aspec s o i s biology
wi h ha o animal spe m, while o he aspec s a e
undamen ally dis inc . Chie among hese is he in ol e-
men o pollina o s in pollen ans e among flowe s in
mos flowe ing plan s (Olle on, 2021). Pollina ion by
animals has my iad consequences o plan ecology and
e olu ion, and as ca ie s o genes and media o s o fi ness
gains h ough pollen expo and eceip , pollen si s a he
e y cen e o he pollina ion p ocess.
Na u al selec ion a ises when pheno ypic ai s a e linked
o indi idual pe o mance and, in u n, fi ness (Opedal, 2021).
“Pe o mance”is used he e in he sense o measu able
quan i ies linking a pa icula kind o pheno ypic ai o
fi ness (A nold, 1983), and “fi ness”in he con ex o
pollina ion usually e e s o ep oduc i e fi ness as measu ed
by seed p oduc ion. The ele an pe o mance componen (s)
can be defined wi h e e ence o he hypo hesized unc ion
o he ai s unde s udy. Fo example, he pe o mance
o indi idual pollen g ains (pollen pe o mance) can be
measu ed as he success in eaching a s igma, ge mina ing,
de eloping a pollen ube ha eaches an o a y, and e ilizing
an o ule (Williams and Maze , 2016). In he con ex o
animal pollina ion, howe e , pollina ion‐ ela ed pe o mance
componen s (pollina ion pe o mance) a e bes unde s ood
Am J Bo . 2023;110:e16200. wileyonlinelib a y.com/jou nal/AJB
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h ps://doi.o g/10.1002/ajb2.16200
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s use, dis ibu ion and ep oduc ion in any medium, p o ided he
o iginal wo k is p ope ly ci ed.
© 2023 The Au ho s. Ame ican Jou nal o Bo any published by Wiley Pe iodicals LLC on behal o Bo anical Socie y o Ame ica.
This a icle is pa o join special issues o he Ame ican Jou nal o Bo any and Applica ions in Plan Sciences:“Pollen as he Link Be ween Pheno ype and Fi ness.”
om he pe spec i e o he pa en al plan and include me ics
such as pollen pickup om pollina o s (a componen o
emale pollina ion pe o mance), placemen on o pollina o s
and subsequen deposi ion on o conspecific s igmas (compo-
nen s o male pollina ion pe o mance). While hese
pe spec i es a e ob iously ela ed, he pollina ion pe spec i e
leads na u ally o ques ions abou flo al ai s unc ionally
in ol ed in he pollina ion p ocess (pollina ion unc ional
ai s), while he pollen pe spec i e leads o ques ions abou
pollen ai s de e mining he a e o he indi idual game o-
phy e (pollen unc ional ai s), such as pollen size and
pollen‐ ube g ow h a es. This dis inc ion is pa ly, bu no
comple ely, aligned wi h he con en ional dis inc ion
be ween p e‐pollina ion and pos ‐pollina ion p ocesses
(Minnaa e al., 2019; Ch is ophe e al., 2020).
As eflec ed in he i le, his special issue ocuses on he
ole o pollen in linking flo al pheno ypes o fi ness.
This idea is summa ized g aphically in he gene al model
ep esen ed in Figu e 1. While his model is on he one
hand concep ual, we will see ha i also can unc ion as an
empi ical oadmap and as a ep esen a ion o an analy ical
amewo k allowing join analyses o many o he p ocesses
discussed in he pape s ha ollow in his special issue. Ou
discussion will cen e mo e on pollina ion pe o mance and
pollina ion unc ional ai s han on pollen pe o mance
and pollen unc ional ai s. This choice pa ly eflec s ou
own esea ch a eas and expe ise and also he ac ha
he pollen pe o mance pe spec i e was well co e ed in a
p e ious special issue o he Ame ican Jou nal o Bo any (see
Fig. 1o Williams and Maze , 2016). In hei in oduc o y
pape , Williams and Maze (2016) also p o ide a b ie
his o ical accoun o esea ch on pollen biology. Ou ocus
is simila o ha o Minnaa e al. (2019), and hei
discussion o “pa hways o pa e ni y” alls na u ally in o he
pollen‐expo pa hway in ou model (Figu e 1).
In he ollowing, we use ou g aphical model (Figu e 1)
as a amewo k o ou lining some o he key opics ela ed
o he ole o pollen in linking flo al pheno ypes o fi ness,
including b ie summa ies o he pape s ha add ess hem
in he cu en special issue. We end by poin ing o gaps in
ou cu en unde s anding and p opose ways o wa d o
add essing hese gaps.
FUNCTION AND PERFORMANCE IN
POLLINATION, OR HOW POLLEN
LINKS FLORAL PHENOTYPE TO
FITNESS
Ou concep ual model (Figu e 1) can be seen as a g aphical
ep esen a ion o a pa h‐analy ical fi ness unc ion linking
pheno ypic ai s h ough hypo hesized causal ela ionships o
componen s o pe o mance and fi ness. This kind o model
bo ows concep ual ideas om W igh ian pa h analysis
(W igh , 1921;Shipley,2016) and can be o malized as a se ies
o s a is ical models yielding es ima es o ai –pe o mance,
pe o mance–fi ness, and ai –pe o mance–fi ness ela ion-
ships. T ai –pe o mance ela ionships a e hose be ween a
pe o mance componen and a ai (e.g., be ween s igma
pollen load and flowe size), and pe o mance–fi ness
FIGURE 1 G aphical model linking classes o pollina ion unc ional ai s (le ) o ep oduc i e fi ness on he igh (W=S
♀
+S
♂
). T acing he a ows
backwa d, he numbe o seeds p oduced as a ma e nal pa en (S
♀
) is a unc ion o he numbe o pollen g ains (P) deposi ed on o s igmas h ough
c oss‐(P
CROSS
) and sel ‐pollina ion (P
SELF
). Because c oss‐pollen eceip equi es pollina o isi a ion, he expec ed c oss‐pollen load can be w i en as a
p oduc o he p obabili y o isi a ion (V) and pollen deposi ion condi ional on isi a ion (P
C
), and he o al pollen load (P)asP=VP
C
+P
S
. Flo al ai s can
indi ec ly inc ease he numbe o pollen g ains (P) by inc easing isi a ion o pollina o s esponding o ad e isemen o ewa d ai s, o di ec ly by
imp o ing mechanical fi and hus he efficiency o pollen ans e . The a e o sel ‐pollina ion is also de e mined by flo al ai s affec ing wi hin‐flowe
pollen ans e . The numbe o seeds si ed h ough pollen expo (S
♂
) depends on he amoun o pollen deposi ed by pollina o s on o conspecific s igmas
(P
DEP
), which in u n depends on a ia ion in pollen placemen on o pollina o s (pollen pickup) as a unc ion o pollina o a ac ion, flowe –pollina o fi ,
and pollen p oduc ion.
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POLLEN AS THE LINK BETWEEN FLORAL PHENOTYPE AND FITNESS
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ela ionships a e hose be ween a fi ness componen and a
pe o mance componen (e.g., how a ia ion in s igma pollen
load ansla es in o seed p oduc ion) (A nold, 1983;
Opedal, 2021). This and ela ed analy ical app oaches a e
gaining inc easing popula i y in e olu iona y ecology (Shaw
e al., 2008;Le check,2016; Henshaw e al., 2020)andp o ide
se e al specific ad an ages in he s udy o pollina ion (S an on
e al., 1991;Conne ,1996;Aigne ,2005; Bols ad e al., 2010;
Opedal, 2021). Mos impo an ly, causal‐in e ence me hods
such as pa h analysis equi e p io knowledge abou he
(hypo hesized) causal ela ions be ween a iables, which is
o en a ailable in pollina ion ecology. Rod íguez‐O e o e al.
(2023)use he ypeo pa h–analy ical fi ness unc ion illus a ed
by ou model o link flo al ai s o se e al pollina ion
pe o mance componen s (pollina o isi a ion, pollen deposi-
ion, pollina ium emo al), and one ep oduc i e fi ness
componen (seed se ) in a se o ood‐decep i e o chids.
I is impo an o keep in mind ha he model
ep esen ed in Figu e 1is no fixed bu can be easily
ailo ed o he biology o he s udy sys em and o he da a
a ailable in a specific s udy. Fo example, in his special
issue, Ga cía‐Muñoz e al. (2023) de eloped s uc u al
equa ion models ha link flo al mo phology, ep oduc i e
in es men (pollen and o ule p oduc ion), and fi ness
(seed p oduc ion) in he sel e E ysimum incanum
s.l. main ained in a pollina o ‐ ee g eenhouse en i on-
men . S uc u al equa ion modeling is closely ela ed o he
fi ness– unc ion app oach desc ibed abo e and allowed he
au ho s o assess suppo o hypo hesized causal ela ion-
ships among a iables. Because he analysis conce ned
plan s kep in a g eenhouse, he fi ness unc ion could be
simplified by omi ing c oss‐pollina ion. Simila ly, o sel ‐
incompa ible species, i would o en be na u al o omi
sel ‐pollen deposi ion om he fi ness unc ion (al hough
sexual in e e ence can ac also in sel ‐incompa ible
species; Webb and Lloyd, 1986). Finally, o simplici y,
ou model ea s sel ed and ou c ossed ma e nal seed
p oduc ion join ly (Figu e 1,pollen‐ eceip pa hway),
which co esponds o emale fi ness as ypically measu ed
in field s udies. A simple ex ension would be o spli his
fi ness componen in o sel ed andou c ossedcomponen s
(e.g., B iscoe‐Runquis e al., 2017).
T ai –pe o mance and pe o mance–fi ness ela ion-
ships can be s udied independen ly (e.g., in field s.
g eenhouse/lab s udies), and subsequen ly combined in o
a comple e fi ness unc ion (A nold, 1983). Indeed, any
s udy explo ing one o mo e links be ween pheno ype,
pe o mance, and fi ness can be seen as es ima ing one
componen ela ionship o a fi ness unc ion. In his sense,
Figu e 1can be seen as an empi ical oadmap whe e he
impo an ole o pollen in all links be ween componen s
helps o cla i y he i le and ocus o his special issue. In
he ollowing sec ions, we gi e se e al examples o how
addi ional ai classes (e.g., pollen mo phology, flo al
shape) and pe o mance componen s (e.g., he e ospecific
pollen deposi ion) can be in eg a ed in o his gene al
amewo k.
Pollen p oduc ion and p esen a ion
Building he kind o fi ness unc ion ep esen ed in
Figu e 1 equi es ca e ul conside a ion o he expec ed
causal ela ions among a iables. F om he male pe spec-
i e, he fi s s ep in success ul c oss‐pollina ion is pollen
placemen by an an he on o a pollina o (“pollen pickup”).
The a e a which his occu s depends on he local
abundance o (po en ial) pollina o s, he o aging p e e -
ences o hese pollina o s, hei mechanical fi wi h he
isi ed flowe s, and he amoun (and pe haps p ope ies) o
pollen p esen ed (Minnaa e al., 2019).
Pollen p oduc ion a ies g ea ly among animal‐
pollina ed plan s, and a long his o y o heo e ical and
empi ical wo k has explo ed he causes and consequences
o his a ia ion. C uden (1977) compiled es ima es o
he a io o he numbe o pollen g ains o o ules
(pollen:o ule a io) o assess and suppo he expec a ion
ha he p oduc ion o pollen ela i e o o ules inc eases
along a g adien om cleis ogamous o highly ou c ossing
species o he ex en ha pollen:o ule a ios can be ea ed
as a eliable p oxy o a ia ion in ma ing sys em. Recen
me a‐analyses, including in his issue, ha e e ealed la ge‐
scale pa e ns and co ela es o pollen:o ule a ios. Fo
example, Cunha and Aizen (2023) es ed and ound suppo
o he expec a ion ha pe ‐flowe pollen p oduc ion
will inc ease wi h flowe display size o compensa e o
inc eased pollen discoun ing when pollina o s isi mul iple
flowe s on he same plan (Ha de and Ba e , 1995).
Also in his issue, Ha de and Johnson (2023) a gue ha
some o he conclusions o p e ious me a‐analyses on his
opic may be p ema u e because he analysis o a ios
can obscu e effec s p esen o one o bo h unde lying
a iables (he e pollen and o ule p oduc ion). Ins ead,
Ha de and Johnson (2023) p opose ha pollen and o ule
numbe s be analyzed join ly in a bi a ia e model, poin ing
ou ha when he analysis is pe o med on a loga i hmic
scale, he pollen:o ule a io can be di ec ly in e ed
om he pa ame e s o such models (gi en ha log Pollen
numbe –log O ule numbe = log [Pollen numbe /O ule
numbe ]). Whe he and how his analy ical app oach will
change he quali a i e esul s o p e ious analyses emains
o be seen, bu his po en ial issue illus a es he impo ance
in biology o ca e ul conside a ion o measu emen s and
hei meaning (Houle e al., 2011). Ha de and Johnson
(2023) also es ed and ound suppo o he hypo hesis ha
pollen numbe pe flowe dec eases in axa wi h mo e
efficien pollen ans e as measu ed by he p opo ion o
pollen eaching s igmas, suppo ing a di ec link om
pollen p oduc ion ia pollen ans e o fi ness, i.e., a
ai –pe o mance–fi ness ela ionship (Figu e 1).
In e ms o wi hin‐popula ion ai –pe o mance ela-
ionships o pollen numbe (Figu e 1), we expec a ia ion
in pollen numbe pe flowe o affec pollen placemen
on o pollina o s and sel ‐pollen deposi ion on o s igmas.
Es ima es o hese ela ionships in na u al popula ions a e
a e, likely eflec ing he gene al ocus on selec ion h ough
POLLEN AS THE LINK BETWEEN FLORAL PHENOTYPE AND FITNESS
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emale unc ion (Minnaa e al., 2019; Ch is ophe
e al., 2020). S an on e al. (1991), in an ea ly applica ion
o pa h analysis in pollina ion ecology, ound ha g ea e
pollen p oduc ion inc eased isi s by small na i e bees,
which in u n led o g ea e si ing success. In one o he ew
s udies quan i ying pheno ypic selec ion on pollen numbe
h ough he male unc ion, Mo gan and Conne (2001)
de ec ed posi i e selec ion. I we assume o now ha pollen
placemen on o pollina o s and subsequen deposi ion on o
s igmas a e co ela ed, his esul indi ec ly suppo s a
posi i e ela ionship be ween pollen p oduc ion and
placemen . This assump ion may no be jus ified, howe e .
Fo example, in his issue, Pea son e al. (2023) epo
posi i e ela ionships be ween indi idual pollen p oduc ion
by Echinacea plan s and placemen on o a ange o
pollina o s, bu his a ia ion was no associa ed wi h
subsequen a ia ion in si ing success. This lack o a
pe o mance–fi ness ela ionship can pe haps be explained
by diffe ences in pollina o beha io and pollen‐ ans e
p ocesses, as discussed below (and see S an on e al., 1991).
In hei analysis o he selfing E ysimum incanum,
Ga cía‐Muñoz e al. (2023) conside ed pa e ns o
co a ia ion among pollen p oduc ion, o ule p oduc ion,
flo al mo phology, and seed p oduc ion. Al hough pollen
numbe had a limi ed di ec effec on seed p oduc ion in a
g eenhouse, his s udy did show ha pollen numbe can
co a y wi h flowe mo phology and wi h o ule p oduc ion,
hus affec ing ep oduc i e fi ness.
Beyond pollen numbe , he dynamics o pollen place-
men on o pollina o s will also depend on he way in which
pollen is p esen ed by flowe s. Fo example, aligning he
daily pe iod o pollen p esen a ion o he ac i i y peak o
pollina o s may bo h op imize pollen emo al and, o some
ex en , educe ep oduc i e in e ac ions wi h co‐flowe ing
species (S one e al., 1998). In his issue, Š enc e al. (2023)
de ec ed alignmen be ween peaks in pollen p esen a ion
and pollina o isi a ion o h ee co‐flowe ing species. Less
is known abou wi hin‐popula ion a ia ion in daily pollen
p esen a ion schedules (Eisen e al., 2017), which would be
an in e es ing ai o include in pollina ion fi ness unc ions
(Figu e 1). Simila ly, plan species diffe in he size o he
pollen “packages” eleased pe pollina o isi . The op i-
mum amoun o pollen eleased pe isi is expec ed o
depend on se e al ac o s (Ha de and Thomson, 1989).
When pollen is he p ima y ewa d, plan s ace he
challenge o a oiding excessi e pollen loss due o g ooming
while ensu ing a ac i eness o pollina o s. In his issue,
Heiling e al. (2023) modeled pollen packaging s a egies
unde he influence o hese cons ain s, confi ming
he expec a ion ha op imum package size depends on
he ela i e p e e ence o pollina o s o la ge packages, bu
also addi ional ac o s such as o al pollen p oduc ion in
he popula ion and possible ela ionships wi h pe ‐plan
isi a ion a es. The ole o pollen as a ewa d in some
species could be easily inco po a ed in o fi ness unc ions
(Figu e 1) by including links om pollen p oduc ion (o
daily p esen a ion) o pollina o isi a ion.
Pollen ans e
Once placed on o a pollina o , pollen can be los h ough a
se ies o fil e s o ba ie s (Minnaa e al., 2019). Fo
example, in he classic s udy o E y h onium g andiflo um
by Thomson and Thomson (1989), less han 1% o he
pollen emo ed om an he s eached a conspecific s igma.
E en in unusually p ecise sys ems such as pollina ium‐
bea ing o chids, pollen is o en los du ing ans e (Capó
e al., 2023; Ha de and Johnson, 2023). These esul s
sugges ha he link om flo al pheno ype (affec ing pollen
placemen ) o male ep oduc i e fi ness ia deposi ion on o
conspecific s igmas may be highly a iable and ha d o
de ec in analyses linking flo al ai s o pollen placemen
(male pe o mance) and numbe o seeds si ed (male
ep oduc i e fi ness, see Pea son e al., 2023). This
a iabili y may be one eason why ela i ely ew s udies
ha e de ec ed pheno ypic selec ion on flo al ai s h ough
he male unc ion (Ashman and Mo gan, 2004; bu see e.g.,
B iscoe Runquis e al., 2017).
Va ia ion in pollen ans e can a ise h ough many
p ocesses, including in e ac ions on he body o he
pollina o (Minnaa e al., 2019). In his special issue,
Moi and Ande son (2023) p o ide empi ical e idence
ha pollen o sequen ially isi ed flowe s can be deposi ed
in laye s on o he pollina o 's body, and ha pollen
deposi ion may decline om ea ly‐ o la e ‐ isi ed flowe s.
Using he ecen ly de eloped fluo escen quan um‐do s
echnique (Minnaa and Ande son, 2019) olabelpollen
o indi idual flowe s, Moi and Ande son (2023)analyzed
he laye s o pollen on he bodies o flypollina o s o
labeled pollen and ound mo e labeled pollen in he op
laye s. When a fly had isi ed wo labeled flowe s, i
ca ied mo e pollen om he fi s flowe han om he
second flowe , sugges ing ha exis ing pollen g ains om
ea lie isi s inhibi addi ional pollen placemen . These
esul s p o ide he fi s empi ical e idence o pollen
laye ing as a mechanism media ing male–male compe i-
ion du ing pollen ans e . How pollen laye ing affec s
subsequen deposi ion on o s igmas emains an open
ques ion.
Ano he impo an sou ce o a ia ion in pollen‐ ans e
efficiency is he iden i y o pollina o s. These diffe ences a e
clea om a small bu g owing body o s udies assessing
landscape‐scale effec s o pollina o mobili y on popula ion
diffe en ia ion (Dellinge e al., 2022; Feigs e al., 2022;
Gamba and Muchhala, 2023). In his issue, Lewis e al.
(2023) used popula ion gene ics o es whe he diffe ences
in he mobili y o hawkmo h and bee pollina o s explain
popula ion diffe en ia ion in wo species o Oeno he a.As
expec ed, hey ound inc eased popula ion diffe en ia ion
wi h less‐mobile pollina o s (bees in hei case), bu li le
effec s on popula ion diffe en ia ion h ough (ballis ic
sho ‐dis ance) seed dispe sal (see also Gamba and
Muchhala, 2020). Fu he mul ispecies s udies assessing
he ela i e impo ance o pollen e sus seed‐media ed gene
dispe sal a e needed o be e unde s and he impac o
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POLLEN AS THE LINK BETWEEN FLORAL PHENOTYPE AND FITNESS
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pollina o declines and changes in pollina o assemblages
on he pe sis ence and e olu ion o plan popula ions.
Besides landscape‐scale effec s o pollina o mobili y,
diffe ences in pollina o o aging pa e ns and beha io may
also affec small‐scale pollen‐ ans e efficiency and si ing
success wi hin popula ions (Minnaa e al., 2019; Ke n
e al., 2023). In wo s udies in his issue, aspec s o
pollina ion efficiency we e compa ed ac oss diffe en bee
species. Pea son e al. (2023) combined field obse a ions,
single‐ isi pollina ion expe imen s and pa e ni y analyses
o show ha bee species diffe en ially influence si ing
success and ha hese diffe ences a e no always cap u ed by
measu es o isi a ion a e o pollen emo al. Simila ly,
Weinman e al. (2023) s udied he composi ion o he pollen
loads ha bees ca y on hei bodies and in hei scopae and
ound ha pollen o many plan species we e packed in bee
scopae (and hus no a ailable o ans e o s igmas)
wi hou occu ing on bee bodies. These wo s udies
accen ua e he alue o combining molecula app oaches
wi h efined pollina ion expe imen s ha go beyond he
me e documen a ion o isi a ion and o s udying bee
o aging s a egies o deciphe sub le p e‐and pos ‐
pollina ion pheno ype–pe o mance–fi ness ela ionships
(Ch is ophe e al., 2020).
Pollina o a ac ion
F om he pe spec i e o he ma e nal plan , he fi s
s ep in success ul c oss‐pollina ion is o a ac a leas one
pollina o indi idual. T ai –pe o mance ela ionships o
pollina o a ac ion ai s a ise when pollina o s make
o aging decisions based on di ec assessmen o ewa d
a ailabili y (Bols ad e al., 2010)o onflo al o plan ‐le el
ad e isemen s ac ing as “hones signals”(e.g., plan
heigh , Lo ie and Aa ssen, 1999;flowe size, A mb us e
e al., 2005). In his issue, ai ‐pe o mance ela ionships
o a ac ion ai s a e demons a ed in wo s udies
o e es ial o chids. Capó e al. (2023)quan ified he
ela ionships be ween plan heigh , flo al display size,
pollina ium emo al, and ui se o fi e species. Al hough
plan size also eflec s o e all igo , which leads o
a ia ion in ep oduc i e success independen ly o polli-
na o s (e.g., T unschke e al., 2017), he posi i e ela ion-
ships be ween pollina ium emo al and hese “ igo ” ai s
also suppo a ole o pollina o ‐media edselec ionin hei
e olu ion. Rod íguez‐O e o e al. (2023) ook heanalysis
o ai –pe o mance–fi ness ela ionships one s ep
u he by de eloping a comple e fi ness unc ion and
using i o es ima e selec ion g adien s. These au ho s also
de ec ed o e all posi i e ai –pe o mance– ela ionships
and selec ion on ad e isemen ai s. In e es ingly, he
ai –pe o mance ela ionships we e compa able be ween
emale (pollen deposi ion) and male pollina ion pe o m-
ance (pollina ium emo al), sugges ing a leas some
connec ion be ween he pollen‐ eceip and pollen‐expo
pa hways o fi ness (Figu e 1).
Flowe –pollina o fi
While he ini ial s ep o he ma e nal plan in ol es
a ac ion o he pollina o , ecei ing pollen hen depends
on he p esence o pollen on he pollina o 's body and on
whe he pa s o he pollina o 's body ca ying pollen make
con ac wi h a ecep i e s igma. To he ex en ha flo al
ai s de e mine he p obabili y o con ac and posi ion
o con ac wi h pollina o bodies, hese flowe –pollina o
fi ai s will hen link flo al pheno ype o pollina ion
pe o mance (Opedal, 2021). Rod íguez‐O e o e al. (2023)
included spu leng h and flowe size as a fi ai in hei
o chid fi ness unc ion and showed ha ai –pe o mance
ela ionships and selec ion on fi ai s end o fluc ua e
d ama ically in bo h s eng h and di ec ion, p esumably
in esponse o a ia ion in flowe –pollina o fi ac oss
popula ions and species isi ed by diffe en pollina o s
(Opedal, 2021). While mos p e ious s udies ha e ocused
on indi idual fi ai s, Dellinge e al. (2023) ook on he
challenge o linking complex flo al shape a ia ion as
de ec ed by mo phome ic echniques o pollen emo al
om an he s and deposi ion on o s igmas. They used a
dimension‐ educ ion echnique, he wo‐block pa ial leas
squa es me hod (Rohl and Co i, 2000), o combine a la ge
se o measu emen s (he e landma ks) in o a single axis
ela ed o a ia ion in pollina ion pe o mance. This
app oach e ealed a de ec able ai –pe o mance ela ion-
ship o pollen emo al om an he s, bu no o pollen
deposi ion on o s igmas. Dellinge e al. (2023) also p o ide
a gene al oadmap o u he wo k along his line.
Pollen placemen on pollina o s is pe haps bes unde -
s ood h ough he lens o pollina ion accu acy (A mb us e
e al., 2009). Fo example, S ewa e al. (2022) compa ed he
p ecision o pollen placemen (one componen o pollina-
ion accu acy) ac oss a di e se se o plan species in
Thailand and ound ha pollen placemen on pollina o s
was mos p ecise in pheno ypically mo e specialized flowe s,
as indica ed (among o he ai s) by bila e al flowe
symme y and used co ollas. In his issue, Pé ez‐Ba ales
and A mb us e (2023) compa ed pa e ns o pollina ion
accu acy ac oss si es whe e Linum species occu ei he alone
o wi h congene s o assess, and o some ex en suppo ,
di e gence in fi ai s among co‐flowe ing species.
When a plan species is isi ed by mo e han one
pollina o species (o unc ional g oup), ai –pe o mance
ela ionships a e likely o diffe among hem. In his
issue, Fu ado e al. (2023) compa ed he pollina ion
efficiency o bee and hummingbi d pollina o s o
Palicou ea igida, le e aging he pollen‐size dimo phism
o hei dis ylous flowe s o assess pollen placemen on
pollina o s and single‐ isi deposi ion on o s igmas. They
ound ha he wo pollina o unc ional g oups diffe ed
in pe ‐ isi pollen deposi ion, especially o he sho ‐
s yled mo ph. Also in his issue, Pea son e al. (2023)and
Weinman e al. (2023)documen diffe ences in pollina-
ion efficiency among bee pollina o axa. These kinds o
diffe ences could be inco po a ed in o fi ness unc ions
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by spli ing he pollen‐deposi ion pe o mance compo-
nen in o pollina o ‐specific con ibu ions (c . Schemske
and Ho i z, 1988).
He e ospecific pollen ans e
Whene e coflowe ing plan s sha e pollina o s, pollen loads
deposi ed on o s igmas may con ain pollen o se e al
species. He e ospecific pollen deposi ion is gene ally
hough o ha e nega i e effec s on seed p oduc ion h ough
mechanisms such as s igma clogging, in e e ence in he
s yle, o conspecific pollen loss (Ashman and A ceo‐
Gómez, 2013; Mo ei a‐He nández and Muchhala, 2019).
In p ac ice, howe e , i pollina o s also end o deposi mo e
conspecific pollen when hey deposi mo e he e ospecific
pollen, inc eased he e ospecific pollen deposi ion may
ac ually co espond o g ea e seed se (e.g., Lopes
e al., 2021), especially i he ecipien species has e ol ed
a deg ee o ole ance o he e ospecific pollen. Fo example,
in his issue, Hao e al. (2023) s udied pa e ns and
consequences o he e ospecific pollen deposi ion on o
s igmas in h ee Silene species and ound ha s igmas
ecei ing mo e he e ospecific pollen also ended o ecei e
mo e conspecific pollen and ha hand‐pollina ion wi h
mix u es o conspecific and he e ospecific pollen did no
usually educe seed p oduc ion compa ed o hose wi h only
conspecific pollen. Such ole ance likely e ol es in esponse
o na u al exposu e o he e ospecific pollen. Fo example,
Mo ei a‐He nández e al. (2023) s udied pollen ans e
wi hin and be ween sympa ic Bu meis e a and compa ed
he effec o expe imen al pollen mix u es among se e al
species ha diffe in he amoun o he e ospecific pollen
hey ypically ecei e in he wild. As p edic ed, a species ha
ecei es mo e he e ospecific pollina ion in he wild appea s
o ha e e ol ed g ea e ole ance o i . How ole ance o
he e ospecific pollen e ol es is no en i ely clea , bu likely
ela es o changes in pollen–pis il in e ac ions and
incompa ibili y sys ems (B oz and Bedinge , 2021).
Analy ically, he e ospecific pollen deposi ion can eadily
be included in o pollina ion fi ness unc ions as a pe o m-
ance componen wi h logical links o pollina o isi a ion
and ad e isemen , ewa d, and flowe ‐pollina o fi ai s
(Figu e 1). As we ha e jus seen, he pe o mance–fi ness
ela ionship (how he e ospecific pollen deposi ion affec s
seed se and he ela ionship be ween conspecific pollen
deposi ion and seed se ) has been well s udied (e.g., Hao
e al., 2023; Mo ei a‐He nández e al., 2023; Pé ez‐Ba ales
and A mb us e , 2023 [all in his issue]) and could easily be
included by modelling seed se as a unc ion o conspecific
pollen deposi ion, he e ospecific pollen deposi ion, and,
p esumably, hei in e ac ion.
T ai –pe o mance ela ionships o he e ospecific pol-
len deposi ion ha e been less well s udied, al hough analyses
o popula ion means sugges ha such ela ionships may
occu a leas occasionally (Peuke e al., 2020; Lopes
e al., 2021). The posi i e ela ionships o en obse ed
be ween conspecific and he e ospecific pollen loads (e.g.,
Tu e al., 2016) also sugges ha he ai –pe o mance
ela ionships migh be simila in shape. Simila
ai –pe o mance ela ionships would mos likely occu i
conspecific and he e ospecific pollen g ains a e placed, on
a e age, on he same pa o he pollina o (Muchhala and
Thomson, 2012). This assump ion may be jus ified in
sys ems wi h sca e ed pollen placemen (e.g., in buzz‐
pollina ion), while in sys ems wi h mo e p ecise pollen
placemen , he e is inc easing e idence o ep oduc i e
cha ac e displacemen ac ing o educe he e ospecific
pollen ans e (A mb us e e al., 1994; G ossenbache
and Whi all, 2011; Eisen and Gebe , 2018). Pé ez‐Ba ales
and A mb us e (2023) s udied he e ospecific pollina ion in
he ligh o local assemblage s uc u e and po en ial
e olu ion o ep oduc i e cha ac e displacemen in co‐
flowe ing Linum species. Thei ocal species, Linum
suff u icosum, occu s in si es wi hou o he Linum species
and in si es wi h co‐flowe ing and pollina o ‐sha ing
congene s. In his sys em, he e ospecific pollen deposi ion
nega i ely affec ed conspecific pollen ube o ma ion, bu
diffe en Linum species we e only pa ially diffe en ia ed in
hei pollina o assemblages and in flo al ai s affec ing
pollen placemen on sha ed pollina o s a sympa ic si es.
Pe o mance–fi ness ela ionships: om pollen
deposi ion o seed se
While male ep oduc i e success equi es pollen expo o
conspecific s igmas, such pollen expo does no necessa ily
gua an ee ha o ules will be e ilized. The ela ionship
be ween conspecific pollen deposi ion and seed p oduc ion
(i.e., he pe o mance–fi ness ela ionship o ou gene al
fi ness unc ion; Figu e 1) is usually asymp o ic, wi h he
asymp o e eflec ing he numbe o o ules and/o he uppe
limi o esou ces a ailable o seed ma u a ion (Ashman
e al., 2004). In e ms o building a fi ness unc ion, he
pollen‐ o‐seeds cu e can be es ima ed ei he in he field o
in a con olled g eenhouse en i onmen , hough he exac
shape may diffe due o he influences o en i onmen al
ac o s in he field (Hildesheim e al., 2019). One sou ce o
a ia ion in pollen‐ o‐seed cu es is he na u e o pollen
compe i ion. A la ge body o wo k has explo ed he
consequences and e olu iona y impo ance o pollen
compe i ion, and we e e eade s o Williams and Maze
(2016) and e e ences he ein.
Pollen unc ional ai s
Beyond pollen numbe , many pollen unc ional ai s
could affec he p obabili y o placemen on o pollina o
bodies, deposi ion on o conspecifics igmas,andcompe i-
i e abili y. T ai s such as pollen size, pollen nu ien
con en , and pollen‐ ube g ow h a e would be s aigh o -
wa d o in eg a e in o a fi ness unc ion (Figu e 1). Pollen
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ai s can also se e o a ac pollina o s when pollen
unc ions as a flo al ewa d. In his issue, Nebaue e al.
(2023) s udied he ole o pollen s e ols in he o aging
decisions, nu i ion, and fi ness o bumble bees. Su p is-
ingly, hey ound ha while bumble bees could de ec pu e
s e ols, hey did no disc imina e be ween diffe en s e ols
o be weenpollenwi hdiffe en s e ol concen a ions.
Analy ically, including pollen nu ien composi ion in o a
fi ness unc ion would likely benefi omdimension‐
educ ion app oaches such as he wo‐block pa ial leas
squa e app oach used by Dellinge e al. (2023)o he
educed‐ ank eg ession app oach ecen ly de eloped o
analyzing ai –pe o mance ela ionships and selec ion on
flo al scen chemis y (Opedal e al., 2022).
Along wi h mo ing game es be ween indi iduals, pollen
can also mo e a hos o diffe en pa hogens. In his issue,
Fe e s and Ashman (2023) e iewed i al plan in ec ions
associa ed wi h pollen, summa izing he cha ac e is ics
o he pollen i ome and i s ansmission, wi h pa icula
a en ion o plan , pollen, pollina o , and landscape ai s
likely o be associa ed wi h a ia ion in i us ansmission.
While he effec o ungal an he pa hogens on pollina ion
has been s udied (Jenne s en, 1988; An ono ics and
Alexande , 1992), oo li le is known abou he effec o
pollen i uses on plan ai s and fi ness o be able o make
clea p edic ions abou i us effec s on pollina ion. In ec-
ions could po en ially affec plan s in ways ha would al e
pollen ans e , c ea ing oppo uni ies o selec ion on flo al
ai s (Giles e al., 2006). In p inciple, such effec s could be
in eg a ed in o a pollina ion fi ness unc ion (Figu e 1).
TECHNICAL ADVANCES IN POLLEN
IDENTIFICATION AND
QUANTIFICATION
S udies o ai –pe o mance–fi ness ela ionships o he
kind discussed abo e o en equi e quan ifica ion and
iden ifica ion o pollen on s igmas o on pollina o s.
Recen ly, me hods o au oma ed pollen iden ifica ion ha e
ad anced conside ably, including machine‐lea ning algo-
i hms o analyzing pollen pho os (Olsson e al., 2021) and
pipelines o me a‐ba coding o pollen samples om bees
(Bell e al., 2016) and he en i onmen (Polling e al., 2022).
A pape in Applica ions in Plan Sciences o ms pa o he
cu en special issue and p esen s a new pollen quan ifica-
ion echnique. Bailey e al. (2023) e alua ed he use o high‐
ene gy iole ligh o pollen g ain classifica ion. The
au ho s sampled pollen pelle s om 16 Apis melli e a hi es
and compa ed iden ifica ion me hods based on high‐ene gy
iole ligh and isible ligh o assess he ela ionship
be ween pollen composi ion and colo . The p o ocol was
able o diffe en ia e 35 pollen pelle colo s and aided in
dis inguishing hei composi ion e en wi hin he same colo
class. This me hod is low‐cos , easy o s anda dize, and
highly ep oducible because pollen colo s can be iden ified
by hei nume ical composi ion (RGB o hexadecimal).
CONCLUSIONS AND PERSPECTIVES
The pape s ha ollow in his special issue a es o he key
ole o pollen in linking flo al pheno ypic a ia ion o
pollina ion pe o mance and ep oduc i e fi ness. We hope
ha ou discussion o he di e se insigh s and esul s
om hese s udies in he ligh o a gene al pa h‐analy ical
concep ual amewo k helps o illus a e he connec ions
be ween opics ha a e o en s udied sepa a ely.
We highligh he alue o a pa h‐analy ical
amewo k o concep ualizing s udies o plan –pollina o
in e ac ions and flo al e olu ion. In s udies ocusing on
one o mo e indi idual ai –pe o mance, ai –fi ness, o
pe o mance–fi ness ela ionship, de eloping a hypo he ical
fi ness unc ion (causal diag am) can aid in e p e a ions by
cla i ying he expec ed links o o he componen s o
pe o mance and fi ness. Because he app oach is modula ,
indi idual ai –pe o mance and pe o mance–fi ness ela-
ionships can be s udied in isola ion and la e linked oge he .
Fo example, se e al s udies included in his special issue
es ima e ai –pe o mance ela ionships by ela ing flo al
pheno ype o pollen placemen o deposi ion in he field
(e.g., Capó e al., 2023;Dellinge e al.,2023; Pé ez‐Ba ales
and A mb us e , 2023;Rod íguez‐O e o e al., 2023). The
co esponding pe o mance–fi ness ela ionship can be
s udied h ough expe imen al manipula ion o pollen loads
in he field o g eenhouse o in e pollen‐ o‐seed cu es
o he influence o he e ospecific pollen deposi ion on he
ela ionship be ween conspecific pollen deposi ion and seed
se (e.g., Hao e al., 2023; Mo ei a‐He nández e al., 2023;
Pé ez‐Ba ales and A mb us e , 2023). While hese kinds
o esul s a e inc easingly a ailable, i is s ill a e o see hem
combined in o a comple e fi ness unc ion o he kind
illus a ed in Figu e 1, and we hope ha his special issue will
inspi e u he wo k along his line.
Two key poin s ha a ise when designing s udies o
ai –pe o mance–fi ness ela ionships a e o conside (1)
he (hypo hesized) unc ion o each kind o pheno ypic ai ,
and (2) he in e media e pe o mance componen s ha link
hese ai classes o ep oduc i e fi ness. I he pollina ion
componen is made only implici by going s aigh
om pheno ype o fi ness, as is o en he case in s udies
o pollina o ‐media ed selec ion (Opedal, 2021), we isk
missing impo an mechanisms such as hose associa ed
wi h pollen loss and male–male in e ac ions du ing pollen
ans e (Minnaa e al., 2019). On his no e, i is common
o see s a emen s abou pollina ion pe o mance compo-
nen s being poo su oga es o p oxies o fi ness. Howe e ,
pollina ion pe o mance componen s a e no necessa ily
s udied because hey a e “p oxies”o ep oduc i e fi ness,
bu because hey in hemsel es a e in o ma i e abou
pollina ion unc ion, which is cen al o unde s anding he
e olu ion o flowe s and plan ep oduc ion. In ac , weak
pe o mance–fi ness ela ionships equally means ha male
ep oduc i e fi ness may be a poo p oxy o pollina ion
pe o mance, highligh ing he impo ance o s udying bo h
componen s.
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Pe spec i es
One gene al insigh om he s udies included in his special
issue and he gene al li e a u e is ha diffe en pollina o axa
may media e diffe en ai –pe o mance–fi ness ela ionships
(e.g., Aigne , 2005; Sahli and Conne , 2011;Fu adoe al.,2023;
Nakazawa and Kishi, 2023; Pea son e al., 2023). One way o
see hisis ha eachpollina o axon media es a unique
pollina ion fi ness unc ion ha can, in p inciple, be es ima ed.
Es ima ing such efined, axon‐specificfi ness unc ions will
equi e c ea i e, mul i‐me hod s udy designs ha d aw on
bo h classical pollina ion–ecological obse a ions, expe imen s,
and molecula echniques (Cas illa e al., 2017). As a s ep in
his di ec ion, i seems impo an o a leas conside
pollina o ‐specific esponses oflo al ad e isemen s and
pa e ns o pollen deposi ion (Schemske and Ho i z, 1988;
S an on e al., 1991).
The de elopmen o new pollen‐labeling echniques
such as quan um do s has opened new oppo uni ies o
quan i ying he a es o pollen g ains a e pollen placemen
on o a pollina o (Minnaa and Ande son, 2019), bu hei
empi ical implemen a ion has been ela i ely slow. We a e
con inced ha such pollen‐labeling me hods will acili a e
s udies o pollen ans e (Ke n e al., 2023) and he sys em‐
specific pe o mance–fi ness ela ionships associa ed wi h
pollen loss du ing ans e (Minnaa and Ande son, 2021).
De ailed pollen acking me hods may also allow us o link
pollina ion pe o mance mo e closely o pollen pe o mance
and hence gain a mo e holis ic unde s anding o when and
why specific pollen g ains a e mo e compe i i ely success ul
han o he s. Combining such app oaches wi h pa e ni y
assessmen s and popula ion gene ics holds u he p omise
o ealis ically es ima ing ai –pe o mance–fi ness ela-
ionships unde he influence o bo h s ochas ic and
de e minis ic componen s o pollen ans e .
Finally,weconcludeby epo ingonaninciden ha
occu ed du ing he p ocess o pu ing oge he his
special issue, which is o ele ance o he b oade
scien ific communi y. Two yea s ago, one o us was
app oached by a o ‐p ofi jou nal wi h he in i a ion o
gues edi a special issue and in i ed he es o us o
con ibu e. In ou p oposal, we explici ly s a ed ou goal
o eaching b oadly ac oss he pollina ion biology
communi y, including young esea che s and esea che s
om he global sou h. A e sending ou in i a ions o
colleagues, we lea ned o he exo bi an p ocessing
cha ges and open‐access publica ion ees ha each au ho
wouldneed oco e ;anamoun ha wouldse e o
exclude he e y g oups we we e ying o each. A e
discussions among ou sel es, some o he au ho s
con ibu ing o his special issue and o he colleagues,
we decided o e ac he special issue om he o iginal
jou nal and ins ead we app oached he edi o ial boa d o
he Ame ican Jou nal o Bo any (AJB) wi h ou special
issue p oposal. A yea and a hal la e , we a e ex emely
happy oha e aken hiss ep.Webelie e ha d awing
b oad a en ion o publica ion bias in o ‐p ofi jou nals,
and he alue o p o essional socie ies and he powe hey
ha e in suppo ing a mo e di e se and inclusi e scien ific
communi y is as impo an as assessing he ole o pollen
in plan ep oduc ion. We hank he edi o s o AJB o he
oppo uni y o publish his special issue and hei suppo
and us h oughou he p ocess.
ACKNOWLEDGMENTS
We hank he mee ing o ganize s and pa icipan s a he
symposium “Towa ds a concep ual ame o s udy flo al
o m and unc ion in pollina ion”o ganized by R.P.B.,
A.S.D., and Ø.H.O. a Ecoflo 2021. Ø.H.O. acknowledges
suppo om he Swedish Resea ch Council (g an n . 2021‐
04777), R.P.B. om he Spanish Minis y o Science and
Inno a ion (g an PID2021‐127264NB‐I00), V.L.G.B. om
Conselho Nacional de Desen ol imen o Cien ífico e
Tecnológico (CNPq, g an n . 308107/2021‐7), and A.S.D.
om he Aus ian Science Fund (g an n . T‐1186).
ORCID
Øys ein H. Opedal h p://o cid.o g/0000-0002-7841-6933
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