Na u al selec ion o ea lie male a i al o b eeding
g ounds h ough di ec and indi ec e ec s in a mig a o y
songbi d
William Velmala
1,2,†
, Samuli Helle
1,†
, Ma kus P. Ahola
1,3
, Ma cel Klaassen
4,5
, Esa Lehikoinen
1
,
Kalle Rainio
1
,P
€
ai i M. Si ki€
a
1,2
& Toni Laaksonen
1
1
Sec ion o Ecology, Depa men o Biology, Uni e si y o Tu ku, Tu ku FI-20014, Finland
2
Finnish Museum o Na u al His o y, Uni e si y o Helsinki, P.O. Box 17, FI-00014 Helsinki, Finland
3
Na u al Resou ces Ins i u e Finland, I €
ainen Pi k€
aka u 3, FI-20520 Tu ku, Finland
4
Depa men o Animal Ecology, Ne he lands Ins i u e o Ecology, D oe endaalses eeg 10, 6708 PB Wageningen, The Ne he lands
5
Cen e o In eg a i e Ecology, School o Li e and En i onmen al Sciences, Deakin Uni e si y, Wau n Ponds, Vic. 3216, Aus alia
Keywo ds
Fi ness, li e his o y, mic oe olu ion, seasonal
in e ac ions, sexual selec ion, iming o
mig a ion.
Co espondence
William Velmala, Sec ion o Ecology,
Depa men o Biology, Uni e si y o Tu ku,
Tu ku FI-20014, Finland.
Tel: +358 50 4085039;
Fax: +358 2 3336598;
E-mail: [email p o ec ed]
Funding In o ma ion
The s udy was inancially suppo ed by he
Academy o Finland (p ojec no. 130436 o
TL). SH was unded by The Tu ku Collegium
o Science and Medicine.
Recei ed: 17 Decembe 2014; Re ised: 19
Janua y 2015; Accep ed: 21 Janua y 2015
Ecology and E olu ion 2015; 5(6):
1205–1213
doi: 10.1002/ece3.1423
†
These au ho s con ibu ed equally o his
wo k.
Abs ac
Fo mig a o y bi ds, he ea lie a i al o males o b eeding g ounds is o en
expec ed o ha e i ness bene i s. Howe e , he selec ion di e en ial on male
a i al ime has a ely been decomposed in o he di ec e ec o male a i al
and po en ial indi ec e ec s h ough emale ai s. We measu ed he di ec ional
selec ion di e en ial on male a i al ime in he pied lyca che (Ficedula hypol-
euca) using da a om 6 yea s and annual numbe o ledglings as he i ness
p oxy. Using s uc u al equa ion modeling, we we e able o ake in o accoun
he empo al s uc u e o he b eeding cycle and he hie a chy be ween he
examined ai s. We ound di ec ional selec ion di e en ials o ea lie male
a i al da e and ea lie emale laying da e, as well as s ong selec ion di e en ial
o la ge clu ch size. These selec ion di e en ials we e due o di ec selec ion
only as indi ec selec ion o hese ai s was nonsigni ican . When decomposing
he di ec selec ion o ea lie male a i al in o di ec and indi ec e ec s, we
disco e ed ha i was almos exclusi ely due o he di ec e ec o male a i al
da e on i ness and no due o i s indi ec e ec s ia emale ai s. In o he
wo ds, we showed o he i s ime ha he e is a di ec e ec o male a i al
da e on i ness while accoun ing o hose e ec s ha a e media ed by e ec s o
he social pa ne . Ou s udy hus indica es ha na u al selec ion di ec ly
a o ed ea lie male a i al in his lyca che popula ion.
In oduc ion
The annual cycle o mig a o y animals in empe a e and
a c ic zones consis s o a leas ou cha ac e is ic pe iods:
b eeding, o e win e ing, and wo mig a o y pe iods
be ween he espec i e b eeding and o e win e ing
g ounds. Mig an s a e aced wi h he inc easing challenge
o iming each o hese pe iods op imally in he ace o
ongoing changes in en i onmen al condi ions (Mølle
e al. 2008b; Ca ey 2009; Knudsen e al. 2011; McNama a
e al. 2011). To unde s and how iming may e ol e in
esponse o hese changes, knowledge abou he way how
selec ion wo ks on he iming o hese phases in he
annual cycle is needed (e.g., Gunna sson e al. 2006;
Go do e al. 2013).
In e i o ial mig a o y bi ds, males usually a i e o
he b eeding g ounds ea lie han emales (Mo bey and
Ydenbe g 2001), which helps hem o claim and es ablish
high-quali y e i o ies (e.g., Aebische e al. 1996; Hassel-
quis 1998; Smi h and Moo e 2005). Ea ly-a i ing males
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
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dis ibu ion and ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly ci ed.
1205
ha e also been ound o a ac highe -quali y ma es (e.g.,
Ala alo e al. 1984; Rubolini e al. 2004), es ablish la ge
ha ems (Hasselquis 1998), and ha e mo e ex a-pai
ma ing oppo uni ies (Reudink e al. 2009; Coope e al.
2011), he eby inc easing hei b eeding success. In addi-
ion, ea ly-a i ing males and emales ha e been shown o
pe o m be e in b eeding in e ms o la ge clu ch sizes,
mo e ledglings (Po i 1998; H€
o ke 2002; T yjanowski
e al. 2004; Se gio e al. 2007), and mo e ec ui ing
o sp ing (Mølle 1994; Hasselquis 1998).
The o e all ad an ages o a i ing ea ly, he e o e, seem
o be well es ablished o bo h sexes, al hough i has been
shown ha a i al da e in he wo sexes may also be
unde di e gen selec ion (Mølle 2007). Howe e , we
ha e gene ally a e y limi ed knowledge on wha he spe-
ci ic selec ion pa hways a e o ea ly male a i al. Few o -
mal analyses using di ec ional selec ion di e en ials ha e
been conduc ed on how na u al selec ion ac s on a i al
ime (Mølle 2007; Mølle e al. 2008a; Tepli sky e al.,
2011; Gienapp and B egnballe 2012; A naud e al. 2013).
Only one s udy has p e iously conside ed he po en ial
di e en pa hways o selec ion on a i al da e, ha is, dis-
inguishing be ween i s di ec e ec s on i ness and i s
indi ec e ec s h ough ea lie laying da e and la ge
clu ch size ha a e likely o depend on he quali y o he
emale (No is e al. 2004). Analyzing da a om Ame i-
can eds a s (Se ophaga u icilla), No is e al. (2004)
ound ha he a i al da e did no ha e a signi ican
di ec e ec on he numbe o ledglings in ei he sex.
Ins ead, he indi ec i ness e ec s o a i al da e, ia
emale laying da e and ledging da e, we e ound o be
signi ican . Howe e , he pa h analysis o No is e al.
(2004) was no used o es ima e he di ec ional selec ion
di e en ial and i s componen s ha a e ele an measu es
when compa ing he s eng h o selec ion be ween species
and ai s (Scheine e al. 2000).
To add ess hese issues, we s udied whe he he e is
selec ion on he iming o male a i al in he pied ly-
ca che (Ficedula hypoleuca), a small mig an songbi d
b eeding in Eu asia and win e ing in sub-Saha an A ica.
We quan i y he selec ion on male a i al da e by calcula -
ing di ec ional selec ion di e en ial using s uc u al equa-
ion modeling (SEM), which enables us o examine o
wha ex en selec ion a ises h ough di e en pa hways
(Scheine e al. 2000). The majo bene i s o applying SEM
in selec ion s udies a e ha i enables (1) he modeling o
a mo e biologically ealis ic scena io o mul i a ia e na u-
al selec ion compa ed o uni a ia e app oaches and mul i-
ple eg ession models (Lande and A nold 1983; Mo issey
2014) and (2) he sepa a ion o selec ion di e en ials in o
di ec and indi ec selec ion and hei componen s (Schei-
ne e al. 2000). In o he wo ds, SEM akes in o accoun
he hie a chical sequence o he di e en a iables, such as
he causally in e ela ed li e his o y e en s du ing a b eed-
ing cycle. This me hod is s ill su p isingly a ely used in
s udies quan i ying na u al selec ion (Mo issey 2014),
despi e i s ob ious bene i s when analyzing mul i a ia e
na u al selec ion om phenomena ha a e empo ally
s uc u ed. To ou knowledge, he e a e no p e ious s ud-
ies ha ha e used his app oach o model he selec ion on
iming o mig a ion in a mig an bi d.
Ma e ials and Me hods
S udy species
The pied lyca che is a long-dis ance mig an , b eeding
in empe a e and bo eal o es s om Wes Eu ope o wes-
e n Sibe ia, and win e ing in wes e n sub-Saha an A ica.
I is a small (weigh ing 16 g on a e age) insec i o ous,
ca i y-b eeding passe ine bi d, which spends eigh mon hs
a yea away om he b eeding a eas, ei he on mig a ion
o in win e ing g ounds in A ica. In Finland, pied ly-
ca che s a i e be ween la e Ap il and ea ly June and he
las bi ds depa by la e Augus . The pied lyca che is an
ex ensi ely s udied model species, as i is abundan
h oughou i s ange and eadily accep s man-made nes
boxes, e en p e e ing hem o na u al ca i ies. (e.g.,
Lundbe g and Ala alo 1992)
S udy si e
Ou s udy si e is si ua ed on Ruissalo, an island o 9 km
2
in he icini y o he ci y o Tu ku (60°260N, 22°100E) in
sou hwes e n Finland. The s udy si e consis s o coni e -
ous o es , mainly sco s pine (Pinus syl es is), and decid-
uous o es , wi h oak (Que cus obu ), sil e bi ch (Be ula
pendula), and small-lea ed lime (Tilia co da a) as he
main ee species. The s udy was conduc ed in 2005–2006
and 2008–2011. Each yea , 230 imbe nes boxes (inside
dimensions 12.5 912.5 cm, inside heigh 23.6 cm,
en ance hole 32 mm) we e a ailable and moni o ed,
excep o 2010–2011 when only 195 nes boxes we e
moni o ed. The nes boxes we e se as lines along pa hs
and oads, he nea es -neighbo nes -box dis ance being
20–40 me e s. Each yea , by he ime he pied lyca che s
a i ed, a p opo ion o he nes boxes was al eady occu-
pied by ei he g ea i s (Pa us majo ) o blue i s (Cyan-
is es cae uleus). The numbe o b eeding pai s o pied
lyca che s in he whole s udy a ea a ied annually, om
79 o 124, wi h a mean o 101 b eeding pai s, al hough
much ewe we e a ailable o he analysis (see below).
The es o he nes boxes we e inhabi ed by i s o
emained uninhabi ed. Pied lyca che nes -box occupancy
o all nes boxes hus a ied om 40.5 o 53.9%, wi h a
mean o 45.9%.
1206 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Selec ion o Ea lie A i al in a Songbi d W. Velmala e al.
Field obse a ions
The a i al da es o indi idual pied lyca che males o
he s udy a ea we e assessed by daily moni o ing o he
whole s udy a ea. The moni o ing co e ed he en i e pe -
iod o he males’ a i al, om la e Ap il un il la e May.
Nes -si e moni o ing was conduc ed be ween 7 AM and 1
PM (UTC +2) by slowly walking h ough he s udy a ea
and s opping a nes boxes, spending 3–4 min in he
icini y o each nes box. The e we e 2–4 obse e s
in ol ed in he moni o ing each day, and each obse e
was andomly selec ed o moni o ing a speci ic subse o
nes boxes on a daily basis.
Flyca che s we e de ec ed using isual and audi o y
cues. The males can be indi idually and unambiguously
ecognized based on he p esence o colo ed and alumi-
num ings, and plumage de ails, including colo a ion o
he back, ump pa e n, shape and size o he whi e o e-
head pa ch, and he amoun o whi e on he ail and
wings. The shape o he o ehead pa ch was cha ac e ized
as a uni o m block, sepa a e do s, o linked do s. The size
o he o ehead pa ch was assigned as la ge, medium,
small, o e y small/absen . Do sal colo a ion was assessed
using a scale om 1 o 7 designed by D os (1936): 1
being black and 7 being emale-like b own. In addi ion o
cha ac e de e mina ion using binocula s, digi al pho og-
aphy wi h a elepho o lens was used o eco d indi idual
plumage de ails in 2010 and 2011.
The a i al da e es ima e is he i s da e a male was
obse ed in he s udy a ea du ing he daily moni o ing.
We included only hose indi iduals ha s ayed b eeding
in he s udy a ea and whose iden i y could la e be con-
i med on plumage cha ac e s while caugh a he nes
box hey we e b eeding in (see easoning below). To
a oid in luencing he males’ e i o y selec ion, hey we e
no apped and inged o o he wise in e e ed wi h du -
ing his pe iod (excep in 2009 when males we e cap u ed
some days a e a i al). Ins ead, each male was s udied
wi h binocula s o indi idual iden i ica ion. Females we e
no included in he s udy because, due o he ex emely
ine di e ences in plumage cha ac e s, hey canno be
eliably iden i ied indi idually, making he de e mina ion
o exac a i al day impossible wi hou in e e ence (i.e.,
ca ching and inging).
The b eeding pe o mance o each male and his ma e
was moni o ed h oughou he b eeding season using he
ollowing indica o s: laying da e, clu ch size, and numbe
o ledged young (Table 1). Bo h adul s we e cap u ed
when he chicks we e 6–7 days old. While in he hand,
he iden i y o a male was con i med o ela e o he same
e i o ial male ha was obse ed in he icini y o he
nes box du ing he a i al pe iod. F om he whole b eed-
ing popula ion, we excluded he ones who abandoned
hei nes o whose nes s we e p eda ed a an ea ly s age
(and hus, hei iden i y could no be e i ied), o who
we e andomly chosen o o he s udy expe imen s ha
migh comp omise ma e choice, clu ch size, o numbe o
ledglings.
S a is ical analyses
We used s uc u al equa ion modeling (SEM), o in his
case pa h analysis, o s udy he s eng h o na u al selec-
ion on male a i al da e, emale laying da e, and clu ch
size by es ima ing di ec ional selec ion di e en ials o
hese ai s (Scheine e al. 2000). The logic o using SEM
in s udies o na u al selec ion is shown in Figu e 1. The
ela i e numbe o o sp ing p oduced ( ledglings) was
used as annual i ness measu e he e. The di ec ional selec-
ion di e en ial is es ima ed by he co a iance be ween a
ai and i ness (Fig. 1). I can be decomposed in o di ec
and indi ec selec ion, which, in u n, may in ol e se e al
di e en pa hways, depending on model complexi y
(Scheine e al. 2000). In SEM amewo k, di ec selec ion
on a ai is es ima ed by summing i s di ec e ec on i -
ness and indi ec e ec s h ough ai s ha go o wa d
owa d i ness in a SEM diag am (Scheine e al. 2000;
Fig. 1). I se e al such media ing ai s a e included in he
model, he indi ec e ec o di ec selec ion can be u he
decomposed in o speci ic indi ec e ec s (Fig. 1). The
di ec e ec o a ai on i ness is he selec ion g adien ,
o he slope o he (pa ial) eg ession coe icien (Lande
and A nold 1983). Indi ec selec ion (o noncausal selec-
ion due o sha ed causes) on a ai is es ima ed by sum-
ming i s e ec s h ough backwa d-going ai s ha a e
connec ed o i ness in a pa h diag am (Scheine e al.
2000). Again, depending on model complexi y and on he
posi ion o a a iable o in e es in a s uc u al model,
indi ec selec ion (like di ec selec ion) can be decom-
posed in o speci ic indi ec e ec s (Fig. 1).
Based on he ecology o mig an bi ds and on he ques-
ions asked in his s udy, we o mula ed an a p io i s uc-
u al equa ion model assuming ha he male a i al da e
Table 1. Desc ip i e s a is ics o he a iables used in he s uc u al
equa ion modeling, pooled o e he whole s udy pe iod. In he selec-
ion analysis, howe e , annual ai means we e used in s anda diza-
ion. In male a i al da e and emale laying da e, he i s e en was
gi en alue he 0, and subsequen e en s a e days a e he i s
e en .
Mean Min–max SD N
% missing
alues
A i al da e 13.40 0–31 5.74 363 –
Laying da e 14.70 0–30 4.42 363 –
Clu ch size 6.56 2–9 0.80 363 –
Numbe o ledglings 5.70 0–9 1.50 261 28.1
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 1207
W. Velmala e al. Selec ion o Ea lie A i al in a Songbi d
has a di ec e ec on i ness as well as an indi ec e ec
on i ness h ough bo h emale laying da e and clu ch size
(Fig. 2). The model also assumes ha he emale laying
da e has a di ec e ec on i ness bu also an indi ec
e ec ia clu ch size and ha clu ch size has a di ec
e ec on i ness only (Fig. 2). Because he ai s included
in ou analysis di e ed in hei measu emen scale and
sample a iance (Table 1), we ollowed He e o d e al.
(2004) o ob ain mean-s anda dized selec ion es ima es
and di ided all ai s (including ledgling numbe o mea-
su e ela i e i ness) by hei annual ai means p io o
analysis. The esul ing mean-s anda dized selec ion coe i-
cien s ep esen he p opo ional change in i ness o a
p opo ional change in he mean o he ai in ques ion.
This makes i possible o compa e ou esul s wi h o he
ai s, popula ions, o species mo e eliably had we used
s anda diza ion based on pheno ypic s anda d de ia ions
(He e o d e al. 2004; Ma sumu a e al. 2012). Howe e ,
mean s anda diza ion equi es a iables wi h na u al o i-
gin ha can be es ablished as equal wi hin di e en s ud-
ies (He e o d e al. 2004). The e o e, o bo h male
a i al da e and emale laying da e, he da e o he i s
e en (i.e., he a i al da e o he i s male o he i s
laying da e o he season) was gi en he alue o ze o and
he subsequen e en s we e sco ed by days since ha
e en on a yea ly basis (Houle e al. 2011). Howe e , we
use e ms “a i al da e” and “laying da e” (ins ead o
“day”) h oughou he a icle in spi e o he abo e-men-
ioned ans o ma ion.
The i o he a p io i model o he obse ed da a was
examined using he chi-squa e es (
2
) and he ollowing
i indices: he oo mean squa e e o o app oxima ion
(RMSEA), s anda dized oo mean squa e esidual
(SRMR), he compa a i e i index (CFI), and he
Tucke –Lewis index (TLI) (Wes e al. 2012). Bo h
RMSEA and SRMR a e badness-o - i measu es, whe e 0
indica es a pe ec i o he model. In con as , in bo h
CFI and TLI, a alue app oaching 1 indica es good model
i (Wes e al. 2012). RMSEA has he added bene i o
p o iding 90% con idence in e als o he es ima e, and
i can be used o es he null hypo hesis ha he es ima e
is <0.5, indica ing a good i (Wes e al. 2012). The
ough cu o alues used o indica e a well- i ing model
o SRMR, CFI, and TLI we e <0.08, >0.95, and >0.95,
espec i ely (Wes e al. 2012). As we had epea ed obse -
a ions o some males (n=42) om di e en yea s, we
used a design-based clus e ing me hod ha co ec s o
nonindependence o da a poin s by adjus ing pa ame e
SEs wi hou explici ly es ima ing his dependency, as ca -
ied ou in mixed modeling (Kal on 1977). Model pa am-
e e s we e es ima ed using obus maximum-likelihood
es ima ion (MLR) ha allows o non-no mal esponse
dis ibu ions (he e, he ela i e ledgling numbe had a
skewness o 1.41 and a ku osis o 2.47), and missing
da a we e handled using ull-in o ma ion maximum like-
lihood (FIML). Analyses we e conduc ed wi h Mplus
( e sion 7.3; Mu h
en and Mu h
en 1998–2012).
Resul s
The a p io i s uc u al equa ion model showed good i o
he da a (n=363,
2ml
=0.24, d =1, P=0.63; RMSEA
(90% CIs) =0.00 (0.00, 0.11), P=0.75; CFI =1.00;
TLI =1.08; SRMR =0.007). The model indica ed s a is i-
cally signi ican di ec ional selec ion di e en ial o ea lie
male a i al da e and emale laying da e and o la ge
emale clu ch size (Table 2). A 10% shi owa d an ea -
lie male a i al da e and emale laying da e gi es an
expec ed p opo ional inc ease in i ness by 0.56% and
0.81%, espec i ely (Table 2). A 10% la ge clu ch size
inc eases i ness by 9.65% (Table 2). The di ec ional selec-
ion di e en ials o male a i al da e and emale laying
da e did no s a is ically di e om each o he (z=0.68,
P=0.50), bu selec ion di e en ial o clu ch size was sig-
ni ican ly s onge han ha o male a i al da e
(z=10.7, P<0.0001) and emale laying da e
(z=10.6, P<0.0001).
Indi ec selec ion o male a i al da e was no de ined
in ou model, and hus, i s di ec ional selec ion di e en-
ial equaled di ec selec ion (Table 2). The es ima es o
indi ec selec ion o emale laying da e and clu ch size
we e e y small and s a is ically nonsigni ican , showing
Selec ion di e en ial
Di ec
selec ion
Indi ec
selec ion
Di ec
e ec s
Indi ec
e ec s
Speci ic (non-causal)
indi ec e ec s
Speci ic (causal)
indi ec e ec s
Figu e 1. The pa i ioning o selec ion di e en ial in o di ec and
(noncausal) indi ec selec ion. Di ec selec ion can be u he
decomposed o di ec e ec s (i.e., selec ion g adien s) and o indi ec
e ec s. Depending on a model s uc u e and complexi y, indi ec
e ec s o di ec selec ion as well as indi ec selec ion can be u he
decomposed o hei espec i e speci ic indi ec e ec s.
1208 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Selec ion o Ea lie A i al in a Songbi d W. Velmala e al.
ha di ec ional selec ion di e en ial o hese ai s was
mainly due o di ec selec ion (Table 2). Selec ion g adi-
en s (i.e., di ec e ec s) o all ai s we e s a is ically sig-
ni ican (Fig. 2; Table 2). The o al indi ec e ec s o
di ec selec ion h ough o wa d media ing ai s included
in he model we e no s a is ically signi ican o any o
he ai s s udied (Table 2), indica ing ha , o example,
selec ion o male a i al da e was owing o i s di ec
e ec on i ness. The pai wise associa ions in he aw da a
be ween all ai s used in he analysis (male a i al da e,
emale laying da e, clu ch size, and numbe o ledglings)
a e shown in Figu e 3.
Discussion
We in es iga ed he s eng h o na u al selec ion on im-
ing o male sp ing a i al in he pied lyca che by aking
ad an age o s uc u al equa ion modeling (SEM). SEM
enabled he ealis ic modeling o selec ion episodes on
empo ally o de ed b eeding ai s. We ound di ec ional
selec ion di e en ial o an ea lie male a i al da e.
Impo an ly, his selec ion coe icien esul ed om he
di ec e ec o male a i al da e on i ness and no om
he indi ec e ec s on i ness h ough emale ai s, ha
is, laying da e and clu ch size. The magni ude o selec ion
on he male a i al da e was simila o selec ion o ea -
lie emale laying da e. Bo h o hese we e, howe e , se -
e al o de s o magni ude lowe han selec ion o la ge
clu ch sizes, which logically a ises om he s ong co ela-
ion be ween clu ch size and numbe o ledglings in he
cu en sample.
A weal h o p e ious s udies has shown co ela ions
be ween he iming o b eeding (i.e., laying da e) and
b eeding success ( o he pied lyca che , see, e.g., Lund-
be g and Ala alo 1992; Canal e al. 2012), including he
associa ions be ween male a i al da e and ep oduc i e
success (e.g., Ala alo e al. 1984; Aebische e al. 1996;
Hasselquis 1998; No is e al. 2004; Rockwell e al.
2012). Howe e , only ew s udies ha e in es iga ed how
na u al selec ion ac s on sp ing a i al da es by quan i y-
ing selec ion coe icien s (Mølle e al. 2008a; Gienapp
and B egnballe 2012; A naud e al. 2013), and e en ewe
ha e examined he pa hways linking a i al ime wi h i -
ness. No is e al. (2004) s udied he Ame ican eds a
and es ima ed he di e en pa hways o selec ion on a i-
al da e o i ness due o di ec and indi ec e ec s, bu
hey did no examine he s eng h o na u al selec ion
(i.e., he di ec ional selec ion di e en ial) o male a i al
da e o o emale ai s. The cu en s udy he e o e
seems o be he i s one ully u ilizing he insigh
ob ained om he SEM o s udying na u al selec ion on
iming o sp ing a i al in a mig an bi d.
Ou esul s show, o he i s ime, a di ec e ec o
male a i al da e on i ness while accoun ing o hose
indi ec e ec s ha a e media ed by po en ial e ec s o
he social pa ne . In o he wo ds, di ec ional selec ion
di e en ial and di ec selec ion o ea lie male a i al
we e due o i s di ec e ec on i ness and no due o i s
Male
a i al
da e
Female
laying
da e
Clu ch
size
Numbe o
ledglings
–0.04 (–0.11, 0.03)
–0.07 (–0.11, –0.03)
–0.06 (–0.11, –0.01)
0.96 (0.78, 1.15)
–0.01 (–0.04, 0.01)
0.26 (0.21, 0.30) 0.01 (0.01, 0.02)
0.05 (0.03, 0.07)
Figu e 2. The s uc u al equa ion model used
o es ima e di ec ional selec ion di e en ial on
male a i al da e, emale laying da e, and
clu ch size. Rela i e numbe o ledglings was
used as a p oxy o i ness. A ows be ween
boxes ep esen assumed causal associa ions
be ween he mean-s anda dized ai s, and
open sho a ows deno e esidual a iances o
dependen a iables. Di ec e ec s (pa hs)
om a ai o i ness can be conside ed
selec ion g adien s. Numbe s in pa en heses
a e 95% con idence in e als.
Table 2. The p opo ional model-p edic ed di ec ional selec ion di e en ial o male a i al da e, emale laying da e, and clu ch size on numbe
o ledglings (i.e., i ness), decomposed in o di ec and indi ec selec ion, whe e di ec selec ion is u he decomposed in o di ec and indi ec
e ec s. Numbe s in pa en heses a e 95% con idence in e als.
A i al da e Laying da e Clu ch size
Di ec ional selec ion di e en ial 0.056 (0.108, 0.005) 0.081 (0.129, 0.034) 0.965 (0.783, 1.147)
Di ec selec ion 0.056 (0.108, 0.005) 0.084 (0.132, 0.036) 0.964 (0.782, 1.146)
Di ec e ec (o selec ion g adien ) 0.059 (0.111, 0.008) 0.070 (0.114, 0.027) 0.964 (0.782, 1.146)
Indi ec e ec s 0.003 (0.003, 0.009) 0.013 (0.034, 0.007) –
Indi ec selec ion –0.002 (0.003, 0.007) 0.001 (0.001, 0.002)
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 1209
W. Velmala e al. Selec ion o Ea lie A i al in a Songbi d

indi ec e ec s ia emale ai s. While emale ai s mos
likely in luence b eeding pe o mance, o example,
h ough iming o laying, clu ch size, and le el o pa en al
ca e, he male a i al da e seems o ha e a di ec e ec on
i ness. Ou esul s hus sugges ha ea ly-a i ing males
a e ei he o a highe pheno ypic quali y, ha e be e
genes, o a e able o gain be e esou ces, such as high-
quali y b eeding e i o y, compa ed o la e -a i ing
males.
A e iew by He e o d e al. (2004) used 38 s udies ha
had epo ed he necessa y in o ma ion o he pos calcu-
la ion o mean-s anda dized selec ion g adien s (o which
nine we e on bi ds). In hose 38 s udies, he median
absolu e alue o mul i a ia e mean-s anda dized selec ion
g adien s was 0.86 o li e his o y ai s, 0.38 o ecun-
di y, and 0.54 o all es ima es (He e o d e al. 2004). The
selec ion g adien s ( he di ec e ec s) o he male a i al
da e and emale laying da e (0.06 and 0.07, espec-
i ely) in ou s udy can hus be conside ed mino . In
con as , he selec ion g adien o clu ch size (0.96) indi-
ca es s ong di ec selec ion. Howe e , compa ing selec-
ion g adien s, o selec ion di e en ials in pa icula
(Scheine e al. 2000), in ou s udy o hose p esen ed in
He e o d e al. (2004) is no s aigh o wa d due o
Figu e 3. Associa ions be ween all ai s used
in he s uc u al equa ion modeling (SEM). All
alues a e s anda dized by hei annual mean.
1210 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Selec ion o Ea lie A i al in a Songbi d W. Velmala e al.
me hodological di e ences. In he cu en s udy, we ha e
aken in o accoun he empo al s uc u e o he pied ly-
ca che b eeding cycle, which gi es a biologically mo e
ealis ic and causally de ined model o na u al selec ion,
whe eas mul iple eg ession models, assuming no such
hie a chy be ween ai s, a e adi ionally used in selec ion
analyses (He e o d e al. 2004; Mo issey 2014). Al hough
no ully excluding he possibili y o equi alen models
(i.e., models assuming a di e en causal s uc u e ha
also show simila i o he da a), ou model i ed he
da a well, sugges ing ha he selec ion es ima es ob ained
can be conside ed o ha e low bias. We he e o e encou -
age u u e s udies o na u al selec ion o use SEM in
o de o base he selec ion es ima es on mo e causally
plausible models o na u al selec ion in he wild.
I should be no ed ha ou s udy only conside s selec-
ion on pa en al ecundi y bu no on su i al. The e may
also be cos s o , and selec ion agains , ea ly mig a ion and
a i al due o ha sh wea he and ood sho age (Mølle
1994; Kokko 1999; B own and B own 2000; Mølle e al.
2008b). Un o una ely, hese a e ex emely di icul ques-
ions o s udy in a small songbi d, such as he pied ly-
ca che , un il i is possible o ack hem indi idually
h oughou hei annual cycle. The impo ance o he
ade-o s be ween he po en ial su i al isks associa ed
wi h ea ly mig a ion and he bene i s o ea ly a i al o
b eeding g ounds hus emain o be s udied. I also
emains o be examined how indi idual condi ion (s a e)
a ec s hese ade-o s: The isk may be mo e modes i
ea ly-a i ing males a e also highe -quali y indi iduals in
he sense ha hey a e mo e likely o ou li e disad an a-
geous condi ions (e.g., Mølle 1994). In ac , he ad an-
age o ea ly b eeding is emphasized when empe a u e
p io o b eeding is low, possibly indica ing highe -quali y
indi iduals o be less in luenced by ha sh condi ions (Ah-
ola e al. 2012).
I can be a gued ha he numbe o ec ui s could ha e
been used as a i ness p oxy ins ead o he numbe o
ledglings, bu se e al au ho s ha e concluded ha ledg-
ling numbe is a ele an i ness measu e (e.g., B omme
e al. 2004) o e en a gued agains assigning i ness ac oss
gene a ions (e.g., Lande and A nold 1983; Che e ud and
Moo e 1994; Wol and Wade 2001). In addi ion, in his
species, he dispe sal dis ibu ion is pa icula ly wide
(Lundbe g and Ala alo 1992; Lehikoinen 2014) and, con-
sequen ly, he numbe s o ec ui s eco ded a pa en al
b eeding g ounds a e low. The e o e, he numbe o
ec ui s is no an app op ia e o eliable i ness measu e
in his species.
In conclusion, we ha e shown ha he e is di ec ional
selec ion o ea ly male a i al o b eeding g ounds in a
mig a o y bi d. By aking in o accoun he sequen ial na -
u e o he ecundi y ai s in ques ion, we es ima ed he
s eng h o selec ion in a s anda dized manne as well as
de ined he speci ic pa hways o di ec ional selec ion o
ea lie male a i al da e. We wan ed o s udy whe he an
associa ion be ween a i al da e and ledgling numbe
migh a ise only h ough emale ai s, such as he laying
da e o clu ch size, bu i does no seem o be so. As ou
s udy emphasizes, he iming o di e en pe iods wi hin
he annual cycle can clea ly be associa ed wi h di ec i -
ness consequences. By s udying how na u al selec ion ac s
on each o hese pe iods, i will be possible o iden i y
wha he ela i e impo ance is o hese pe iods o bi ds,
and gain impo an knowledge o e alua ing he po en-
ial o mig an s o cope when he en i onmen changes.
Acknowledgmen s
We hank Sa a Calhim, Joe He e o d, and Ha y Ko hals
o hei help wi h he s udy. Suzanne Collins om he
Uni e si y o Tu ku G adua e School (UTUGS) made
nume ous co ec ions o he manusc ip . The s udy was
inancially suppo ed by he Academy o Finland (p ojec
no. 130436 o TL). SH was unded by The Tu ku Colle-
gium o Science and Medicine.
Con lic o In e es
The au ho s decla e hey ha e no con lic o in e es s.
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