Ecology and E olu ion 2017; 7: 665–673  
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665
www.ecole ol.o g
Recei ed:22Augus 2016
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Re ised:24Oc obe 2016
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Accep ed:5No embe 2016
DOI:10.1002/ece3.2658
ORIGINAL RESEARCH
La i udinal a ia ion in sexual dimo phism in li e- his o y ai s
o a eshwa e ish
Sa u Es lande 1 | Kimmo K. Kahilainen1 | Jukka Ho ppila1 | Mikko Olin1 |
Ma i Rask2 | Jan Kubečka3 | Jiří Pe e ka3 | Milan Říha3 | Hannu Huuskonen4 |
Leena Nu minen1
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.
© 2016 The Au ho s. Ecology and E olu ionpublishedbyJohnWiley&SonsL d.
1Depa men o En i onmen alSciences/
Aqua icSciences,Uni e si yo Helsinki,
Helsinki,Finland
2Na u alResou cesIns i u eFinland,
Jy äskylä,Finland
3BiologicalCen e,Academyo Scienceso 
heCzechRepublic,Hyd obiologicalIns i u e,
ČeskéBudějo ice,CzechRepublic
4Depa men o Biology,Uni e si yo Eas e n
Finland,Joensuu,Finland
Co espondence
Sa uEs lande ,Depa men o En i onmen al
Sciences/Aqua icSciences,Uni e si yo 
Helsinki,Helsinki,Finland.
Email:[email p o ec ed]
Funding in o ma ion
Uni e si yo Helsinki;R.E ikSe lachius
Founda ion;Be gs åde B o Se lachius
Founda ion
Abs ac
Sexualdimo phismiscommonac oss heanimalkingdom,bu  hecon ibu iono en-
i onmen al ac o sshapingdi e encesbe ween hesexes emainscon o e sial.In
ec o he ms,li e-his o y ai sa eknown oco ela ewi hla i ude,bu sex-speci ic
esponsesa eno wellunde s ood.Weanalyzedli e-his o y ai  a ia ionbe ween
hesexeso Eu opeanpe ch(Pe ca lu ia ilisL.),acommon eshwa e  ishdisplaying
la ge  emalesize,byemployingawidela i udinalg adien .Weexpec ed o indsex-
dependen la i udinal a ia ioninli e-his o y a iables:leng ha age,leng hinc e-
men ,andsizea ma u i y,wi h emalesshowingconsis en lyhighe  alues hanmales
a allla i udes.We u he an icipa ed ha  hisgende di e encewouldp og essi ely
dec easewi h heinc easinglyha shen i onmen alcondi ions owa dhighe la i ude.
Wehypo hesized ha g ow handleng hinc emen woulddec easeandsize/agea 
ma u i ywouldinc easea highe la i udes.Ou  esul scon i med emale-biasedsex-
ualsizedimo phisma allla i udesand hemagni udeo sexualdimo phismdimin-
ished wi h inc ease in la i ude. G ow h o  bo h sexes dec eased wi h inc ease in
la i ude,and he emalela i udinalclineswe es eepe  han hoseo males.Hence,we
challenge wop edominan ecological ules(Rensch’sandBe gmann’s ules) ha de-
sc ibecommonla ge-scalepa e nso bodysize a ia ion.Ou da ademons a e ha 
hese wo ulesa eno uni e sallyapplicableinec o he mso  emale-biasedspecies.
Ou s udyhighligh s heimpo anceo sex-speci icdi e encesinli e-his o y ai s
alongala i udinalg adien ,wi he iden implica ions o awide angeo s udies om
indi idual oecosys emsle el.
KEYWORDS
Be gmann’s ule,g ow h,pe ch,Rensch’s ule,sex,sexualma u i y
1 | INTRODUCTION
Sizedi e encebe ween hesexesisacommonphenomenonamong
animals,bu p onouncedin e -andin aspeci ic a ia ionexis sin he
magni udeo sexualsizedimo phism(SSD)(Blanckenho n,S illwell,
Young, Fox, & Ash on, 2006; Cox, Ba e , & John-Alde , 2008).
Se e al heo ies ha e a emp ed o explain he a ia ion in SSD
by di e en  ac o s including sex-dependen  di e ences in sexual
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selec ion, ulne abili y o p eda o s, niche seg ega ion, and pa en-
alin es men (Abouhei &Fai bai n,1997;Renniee al.,2008).The
egula iono SSDiscomplexbecauseeacho  hese ac o smaycon-
s aino ampli y hedeg eeo dimo phism(Shine,1989),andi iss ill
unclea how hesedi e en  ac o sde e mine he a ia ioninsexual
dimo phism(Mandikie al.,2004;Young,2005).Onep ominen mac-
oecologicalpa e nis heRensch’s ule(Rensch,1950),whichs a es
ha  hemagni udeo SSD ends oinc easewi hinc easeinbody
sizewhenmalesa e hela ge sexand odec easewi hinc easein
sizewhen emalesa ela ge (Fai bai n,1997). Consequen ly,male
bodysize a iesmo e han emalebodysize,i espec i eo which
sexisla ge .Rensch’s uleholds o a a ie yo animal axa, o ex-
ample,insec s, ep iles,bi ds,andmammals(Blanckenho n,Meie ,&
Tede ,2007;Fai bai n,1997).Howe e , hemechanismsunde lying
Rensch’s ule emainobscu e,and he uleappea s obemo econ-
sis en in axawi hmale-biasedSSD hanin axawi h emale-biased
SSD(Webb&F eckle on,2007).
A gene al assump ion is ha  esponse o  sexes is simila  o
changesinen i onmen ,bu somes udiesha eshowndi e en ial
sensi i i y o  males and emales o en i onmen al ac o s such as
empe a u e(Fai bai n,2005), huspo en iallyp omo ing a ia ion
in SSD. When en i onmen al condi ions imp o e, he sex ha  is
mo esensi i emayachie eop imalsizemo e eadily haninpoo e 
condi ions esul inginaninc easeinSSD(Vedde ,Dekke ,Visse ,
&Dijks a,2005),hence,consis en o coun e  oRensch’s ulede-
pendingwhichsexismo esensi i e.Fo example,la geindi iduals
equi emo e ood oa ainla ge sizeand omain ainbody unc ions
(Blanckenho n,1998),anda elikelymo esensi i e o he mal a i-
a ion ia hei highe me abolic a es(Pö ne &Peck,2010).Thus,
his ollows ha changesin heen i onmen ,suchasla i udinal a i-
a ion,mayha eag ea e impac on hela ge sexinSSD-displaying
species.
WhileRensch’s uleexplains he ela ionshipbe weenbodysize
andex en o SSD,ano he well-knownecological ule,Be gmann’s
ule (Be gmann, 1848; e . in James, 1970) desc ibes geog aph-
ical size a ia ion. In addi ion, as Rensch’s ule depends on body
size a ia ion,i hasbeensugges ed ha Be gmann’s(o con e se
Be gmann’s) ule may ela e o sexual size di e ences and hei 
pu a i e selec i e causes (Blanckenho n e al., 2006). Be gmann’s
ules a es ha  hebodysizeo awidelydis ibu edanimalclade
inc easeswi hla i ude.While hedi ec applicabili yo Be gmann’s
uleisunes ablished(Blanckenho ne al.,2006; Mei i,2011), he
consensus is ha  la i udinal body size a ia ion is e iden ly con-
nec ed o empe a u e(Blanckenho n&Demon ,2004).Theusual
explana ion ende ed o Be gmann’s uleis ha la geanimalsexpend
lessene gy o  he mo egula ion,becauseo  hei smallsu ace- o-
olume a io,and he e o e,la ge indi idualsizeis a o edincolde 
clima es.Be gman’s ulewasini ially o mula ed o endo he mican-
imals,andi sex apola ion oec o he msiscon o e sial(Ash on&
Feldman,2003).In ac ,opposi eclinesinbodysizes(i.e.,con e se
Be gmann’s ule) a e common in many ec o he ms, such as ogs
andsalamande s(Adams&Chu ch,2008;Miaude al.,2001),and
inse e al ishspecies,bodysizedec eases owa d hepoles(New,
Hulme,&Jones,1999;Vázquez& S e ens,2004). Inec o he ms,
suchas ish, he empe a u e-associa edsho e g owingseasona 
highe la i udesmaylimi bodysize(Blanckenho n&Demon ,2004).
Howe e , Be gmann’s ule o  ish is s ill ela i ely unde  s udied
(Rypel,2014).
In e mso g ow ho bodysizeplas ici y, isha eanin e es -
ingg oupbecause ishdisplayallome icg ow h,whichenablesa
as e  esponse o changing en i onmen al condi ions ela i e o
manyendo he micanimals(A nold,Ru ,&Kun z,2006;Woo on,
2012).Tempe a u e is he mos  impo an  en i onmen al a iable
go e ningme abolicac i i y(B own,Gillooly,Allen,Sa age,&Wes ,
2004)andinducesconside ablepheno ypicplas ici yinbodysize
o  ec o he mic animals (Angille a & Dunham, 2003). Gene ally,
g ow ho  ishinc easeswi hinc easein empe a u e oaspecies-
speci ic op imum alue, dec easing he ea e  (Woo on, 2012).
Op imal empe a u e o g ow hmaychangewi hageandsize,as
ju enilesgene allyp e e highe  empe a u es hanadul s(Pede sen
&Jobling,1989).
Teleos  ish species display p edominan ly emale-biased SSD
(Webb&F eckle on,2007).As hegonadsizeo  emalesgene allyin-
c easesmo e apidlywi hsize han ha o males(Hende son,T i edi,
&Collins,2000),la ge emalesa eespeciallyimpo an inpopula ion-
le el ep oduc ion(Oline al.,2012;Ven u ellie al.,2010).Acco ding
o he ecundi yad an agehypo hesis(Da win,1871;Shine,1978),
emale-biasedSSDisdue oselec ion a o ingala gebodysize o
ensu ehighe  ep oduc i esuccess,whichalsoleads o hein e seo 
Rensch’s ule(Fai bai n,1997).
He e,weanalyze hela i udinal a ia ioninsexualdimo phism
inli e-his o y ai s inEu opeanpe ch(Pe ca lu ia ilis L.) byusing
a comp ehensi e ield da a om co e dis ibu ion (50ºN) o he
no he ndis ibu ionlimi (69ºN).Pe chisoneo  hemos common
eshwa e  ish species ac oss Eu ope (38–69°N), inhabi ing len ic
habi a s omponds o hela ges lakes(Ko ela &F eyho ,2007).
I isacool-wa e sp ing-spawningspecieswi hanop imumg owing
empe a u eo ca.23°C(Méla d,Kes emon ,&G igna d,1996)anda
maximumleng ho 60cm,bu mo e ypicallya ainingaleng ho up
o25cmdependingonlakeandpopula ion ype(Ko ela &F eyho ,
2007).Thegene alli e-his o y ai so pe cha ewellknownanddoc-
umen edinse e alpape s (Heibo,Magnhagen,&Vølles ad,2005;
LeC en,1951;Tho pe,1977).Pe chdisplays emale-biasedsexual
dimo phism in size, g ow h, and ma u a ion (Heibo & Magnhagen,
2005;Méla de al.,1996),bu  hesex-speci icla i udinalpa e ns
a ela gelyunknown.
Weexpec ed ocon i msexualdimo phismo g ow handma u-
i yo pe cha alls udiedla i udes.As heene gydemando  emale
pe chishighe  han ha o males(Malison,Bes ,Kayes,&Amundson,
1985),inaddi ion o hehighe sensi i i yo  emales o he mal a i-
a ion(Es lande e al.,2015),weexpec ed emales oshowas eepe 
la i udinal a ia ioning ow h.Thus, his ollows ha sex-speci icdi -
e encesin g ow hand sizewoulddec ease owa dhighe la i ude
andwould p oduce a pa e n o  SSD con a y o he p edic ion o 
Rensch’s ule.Finally,possibleexplana ions o obse edpa e nso 
SSDa ediscussed.
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2 | MATERIALS AND METHODS
2.1 | Sampling
Da awe ecollec ed om25wildpe chpopula ionsalongala i udinal
g adien (50°–69°)wi hmul imeshgillne s(Eu opeanS anda dGillne 
SamplingEN14757;mesh ange5.25–60mm)du ing2000–2012a 
heendo  heg owingseason(Augus -Sep embe )(Table1).Bo hli -
o alandpelagialwe esampled oassess he pu a i ep esenceo 
di e gen pe chmo phs(S anbäck&Eklö ,2003).Howe e ,wedid
no  indsignso pe chpopula iondi e gence.Theda aincluded2736
indi iduals:1139males(42%)and1597 emales(58%)(Table1).A 
la i udes om 69 o 50°N, he annual a e agewa e  empe a u es
inc ease om2 o9°C(S ašk aba,1980)and heleng ho  heg ow-
ing season om 110 o 190days (Rö ze  & Chmielewski, 2001).
La i ude, longi ude, al i ude, lake su ace a ea, and o al phospho-
usconcen a ionwe emeasu ed omalls udylakes.Wa e quali y
pa ame e s,suchaswa e  anspa ency, ha is,Secchidep h(a e -
ageo alllakes,3.6m±2.2SD)andpH(6.9±0.3m) a ied,bu we e
no s a is icallysigni ican be weenla i udes(p<.05).All hesampled
lakesa emul ispecies,andspeciesdi e si yand ishdensi y a ybo h
be weenlakesandla i udes.
2.2 | Leng h inc emen , ma u i y, and sexual
size dimo phism
Sex, o alleng h(accu acy1mm),andweigh (0.1g)we emeasu ed,
andope culawe ecleaned o ageandback-calcula edg ow hde-
e mina ions(Bagenal&Tesch,1978).Theleng ho agea ma u i y
da awasno a ailable o allo  helakess udied,bu leng handage
a ma u i ya eknown oco ela eposi i elywi hla i udeinpe ch
(Heibo,2003;Heiboe al.,2005).As heda aanalyzedhe eshowed
asimila pa e n,agea ma u i ywases ima edacco ding oHeibo
(2003)bylinea  eg ession:agea ma u i y=−1.2+0.04×la i ude;
R2=.59,p < .005,and hesewe eused oassess heleng ha ma u-
i y omcu en da a.Theback-calcula edg ow ho pe chwasde-
e mined om heo oli ho ope culumbone o eachindi idualusing
heMonas y skyme hod:nonlinea  ela ionshipbe ween heo oli h/
ope culum adiusand o alleng ho  he ish(Bagenal&Tesch,1978):
Li = (Si/Sc)b × Lc,
whe e Li, Si=leng ho  isha  o ma iono i: h adiuso  adiusa age
i; Lc, Sc=leng ho  isho  adiusa  he imeo cap u e;andb =g ow h
coe icien i.e. heslopeo  he ela ionshipbe weeno oli h/ope cu-
lum adiusandleng h.
The be ween-sex and la i udinal di e ences in he annual (a)
leng hinc emen sand(b)leng ha agewe eanalyzedwi hanalysis
o  a iance o  epea edmeasu es(ANOVAR),andda ausedwe e e-
s ic ed oageg oups1–6(n=2004),becauseolde  ishwe e a eo 
absen  omsou he npopula ions(50°).In heANOVARmodels,sex
( wole els)andla i ude( ou le els)we econside edas ixed ac o s.
Mauchly’s es indica ed ha  heassump iono sphe ici yhadbeen
iola edinbo hmodels,(a)
x2
(14)
=
5699.44
,p > .05;(b)
x2
(14)
=
332.44
,
p > .05,and he e o e,deg eeso  eedomwe eco ec ed(e.g.,Field,
TABLE1 Summa yo la i udinalpe chmeansizeandage(±SD)da ausedinanalyses(CZE=CzechRepublic,SFI=Sou he nFinland,CFI=Cen alFinland,NFI=No he nFinland).Lake
cha ac e is ic alues ep esen  hemean aluespe la i ude,wi ha angeinpa en heses
Popula ion o igin Lake in o ma ion Fish da a me ics
La i ude (ºN) Longi ude (ºE)
Al i ude
(m a.s.l.) Popula ions (n) Lake size (ha)
Mean dep h
(m) To P (μg L−1)
Pe ch
Indi iduals (n) Female (%)
To al leng h
(mm) Weigh (g)
Age
(yea s)
50 16 240 4(CZE) 120(60˗250) 17(14˗23) 44(10˗80) 668 58 180±2 96±5 4±0.6
60 25 130 6(SFI) 270(20˗700) 5(3˗6) 21(5˗40) 516 60 150±2 51±3 3±0.9
63 29 150 6(CFI) 230(20˗470) 4(4˗5) 10(5˗14) 350 62 160±3 63±4 4±0.1
69 26 200 9(NFI) 13660(350˗104300) 8(3˗14) 7(4˗21) 1202 56 193±2 109±3 6±0.5
668
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2013)usingG eenhouse–Geisse es ima eso sphe ici y(a)(p = .280);
(b)(p = .872).
Ra ios o sexualdimo phismindices(SDI)we ecalcula edusing
heme hodo Gibbons(1992):
(A/B)−1,
whe eAis hemeansizeo  hela ges sexandBis hemeansize
o  hesmalles sex.Sex-speci icmeansizes o SDIcalcula ionwe e
weigh ed by numbe  o  indi iduals wi hin age g oups (2–10yea s)
whenlake-speci icsubsamples ep esen ed ueleng handagedis-
ibu ionineachlake; hus,oneSDI aluepe popula ion(in o al25)
wascalcula ed.S epwisemul iple eg essionswi h o wa dselec ion
o  a iableswe eused oiden i y hemos impo an en i onmen-
al a iablesexplaining he a ia ioninSDIs.En i onmen al a iables
(la i ude, longi ude, al i ude, lake su ace a ea, and o al phospho-
usconcen a ion)we een e edin hemul iple eg essionanalysis,
i  p < .05. The s a is ical analyses we e pe o med using IBM SPSS
S a is ics o Windows, e sion21.0(IBMCo p.,A monk,NY,USA).
3 | RESULTS
3.1 | G ow h
Thela i udinal a ia ionso leng ha age(ANOVAR;F[3,924]=6.92,
p < .001)andleng hinc emen (ANOVAR;F[3,924]=2.10,p = .010)o 
pe chwe e sex-dependen  (Figu e1).O e all, he g ow ho  pe ch
dec eased wi h inc ease in la i ude (ANOVAR; F[3,924] =131.07,
p < .001),and heleng ha  ageo  emaleswasla ge  han ha  o 
malesa allla i udes(ANOVAR;F[1,924]=36.48,p < .001)(Figu e1).
Howe e , heleng ha ageandleng hinc emen di e encebe ween
sexes a ied,dependingonla i udeandage(Figu e1;Table2).A la i-
ude50°N, heleng ha age o  emaleswasla ge  han o malesinall
ageg oups(ANOVAR;F[5,384]=14.99,p < .001)(Table2),and hean-
nualleng hinc emen washighe in emales haninmales(ANOVAR;
F[1,84] =14.38,p < .001),despi enosex-dependen di e encesinage
g oups2 and 6(Table2; Figu e1). A la i ude 60°N, emaleswe e
o e allla ge  hanmales(ANOVAR;F[5,76] =5.54,p = .012),indica ed
bysex-dependen di e encesinageg oups2–6(Table2;Figu e1).
No signi ican  sex dependency on annual leng h inc emen s in he
la i ude60ºNinc emen wasde ec edwhenpoolingallageg oups
(ANOVAR;F[1,76]=3.02,p = .086);howe e ,asex-dependen di e -
encewasobse edinageg oups4and5(Table2),wi hg ow ho 
emalesbeing as e  han ha o males(Figu e1).A la i ude63°N,
emaleswe ela ge (ANOVAR;F[5,106]=4.72,p = .02)andg ew as e 
(ANOVAR;F[1,106]=4.57,p = .035) hanmaleswhenallageg oups
we epooled,indica edbysex-dependen di e encesinleng ha age
andleng hinc emen in heolde ageg oups(g oups4–6)(Table2;
Figu e1).Whenallageg oupswe epooleda  heno he nmos la i-
ude69°N, emales we ela ge  (ANOVAR; F[5,658]=5.26,p = .012)
and g ew as e  (ANOVAR; F[1,658]=4.09, p = .043) han males
(Figu e1),indica edbysex-dependen di e encesinleng ha agein
ageg oups5and6(Table2)and heannualleng hinc emen inage
g oups1,3,5,and6(Table2).Ingene al, heannualleng hinc emen 
FIGURE1 A e ageannual o alleng hinc emen s( op)anda e age o alleng ha age(bo om)wi hs anda dde ia ion(±SD)o  emale
(openci cles)andmale(black iangles)pe cha la i udes50–69°N
Age (yea s)
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ESTLANDER ET AL.
showed dispa a e la i udinal clines; he sou he nmos  popula ions
had he as es g ow hin heea lyyea so li eand heno he nmos 
popula ionsinla e yea s(Figu e2a,b).Addi ionally,in he i s yea 
o li e,ag ea e p opo iono o e allg ow hwasa ainedby emales
ela i e omales,whe easinolde indi iduals, heopposi e endwas
obse ed(Figu e2a,b).
Whenpoolingallageg oupsandbo hsexes, hemaximumleng h
o  pe ch dec eased wi h inc ease in la i ude (420, 365, 344, and
332mma la i udes50,60,63,and69°N, espec i ely).Thea e age
leng h a iedsigni ican lybe weenla i udes(ANOVA,F[3,2736] =95.59,
p < .001),bu wi hou aclea la i udinal end(Table1).
3.2 | Longe i y and ma u i y
Thea e ageage a iedsigni ican lybe weenallla i udes(ANOVA,
F [3,2736]=177.53; p = .001), as he oldes  ish we e ound a  la i-
ude 69°N and younges  a  la i ude 60°N (Table1). Males we e
1.2–1.5yea s younge  han emales a  la i udes 60, 63, and 69°N
(ANOVA;F[3,2728]=17.69,p < .001),bu a la i ude50°N, hea e age
ageo  emalesandmaleswas hesame.Theagea ma u i yinc eased
om 2 o 5yea s wi h inc ease in la i ude, and he co esponding
leng ha ma u i yinc easedca.50mm o bo hmales(126–180mm)
and emales(138–190mm)(Table3).
3.3 | Sexual size dimo phism
In hes epwisemul iple eg essionmodel,o he en i onmen al ac-
o s ailed oen e  he eg essionequa iononcela i udewasincluded
(Table4).Thedeg eeo sexualsizedimo phismo pe chdec eased
wi hinc easeinla i ude,andla i udesigni ican lyp edic edSD indi-
ces(Figu e3)(R2 =.84;F = 93.33;p < .001),indica ing ha  hesizedi -
e encebe weensexeswasin e selyassocia edwi hla i ude.
4 | DISCUSSION
Asexpec ed,allpe chpopula ionss udiedexhibi edsigni ican sexual
dimo phisming ow h,size,andma u i y,wi h emalesg owingla ge 
andma u ingla e  hanmales.G ow ho bo hsexesdec easedand
heleng ha ma u i yinc easedwi hla i ude,bu la i udinal ends
we e gene ally s eepe  in emales han in males. Acco dingly, he
magni ude o  SSD diminished in conce  wi h inc ease in la i ude,
sugges ing s onge  sensi i i y o  emales o la i udinal a ia ion,
because emalebodysizeshowedaninc easedplas ici y ela i e o
males.Thus,pe chdidno  ollowRensch’s ulein hep esen s udy,
bu showed heexac con e sepa e n.Incon as ,ou  esul sa e
consis en  wi h he concep ion ha  g ow h esponse can be sex-
speci ic o en i onmen al condi ions (Bondu iansky, 2007; S illwell,
Blanckenho n,Tede ,Da idowi z,&Fox,2010).Inaddi ion,s udies
ha desc ibe hein e seo Rensch’s ule(e.g.,Fai bai n,1997)sug-
ges  ha  SSD esul s om ecundi y selec ion a o  la ge  emale
size.Thislikelyholdsalso o pe ch,because he ecundi yo pe ch
inc easeswi h emalebodysize(Oline al.,2012).
Se e al ac o s inducing gende -speci ic di e ences in g ow h
ha ebeenp oposed,includingene gyalloca ion, isk- aking,and ul-
ne abili y op eda o sandpa en alin es men (Renniee al.,2008).
Mo e ecen ly,sex-speci icdi e enceso pe chha ebeenobse ed
ingu mic obio alinked odis inc die a yp e e ences(Bolnicke al.,
2014)andmay husha e u he implica ionso ene gy ou ingand
indi idualme abolism.Due o hedi e en demands o ene gyacqui-
si ion,malesand emalesmayha e a iables a egies o  ade-o s
be ween ood acquisi ion and p e ailing en i onmen al condi ions
(Hol by & Healey, 1990). In op imal en i onmen al condi ions (e.g.,
clea  wa e  o  o aging, op imal empe a u e, low p eda ion p es-
su e), emalesin es inac i e eeding oensu esoma icg ow hand
la e gonadosoma icg ow h,whe easmalesdono need oin es as
muchin eedingand as g ow h,asspe mislessene gy-demanding
op oduce(Renniee al.,2008).The e o e,changesinop imal eeding
condi ionsha e hemos p onouncede ec son hemos ac i e eed-
e s,which a e o en emales (Es lande  e al., 2015; Ho ppila e al.,
2011),whe easmalesneed og owonly osizea sexualma u i y.
Consequen ly,con adic ingwi hRensch’s ulewhichimplies ha sex-
ualselec ionis hemaind i ing o ceunde lyingSSD(Fai bai n,2005),
wesugges  ha di e en  o cesbeyondsexualselec ion,suchassex-
speci ic esponses o a ia ioninen i onmen alcondi ions,maybe
also esponsible o shapingSSDpa e nsinpe ch.
Inaddi ion ola i udinal a ia ioninSSD,pe chdisplayedano e -
alldec easingg ow hin e mso leng hinc emen wi hinc easein
la i udei espec i eo sex.Thisisinlinewi hHeiboe al.(2005),who
sugges ed ha pe ch ollow hecon e sepa e no Be gmann’s ule
TABLE2 p- alues om epea edmeasu emen sanalysiso  a ianceinbe ween-sexcompa isonso annual o alleng hinc emen sand
leng ha ageo pe cha la i udeso 50–69°N.Signi ican  alues(p<.05)a einbold
Age (yea s) and
sample size
La i ude (°N)
50° 60° 63° 69° 50° 60° 63° 69°
Annualleng hinc emen s Leng ha speci icage
1(n=292) 0.0323 0.6873 0.1878 0.0158 0.0323 0.6873 0.1878 0.2050
2(n=293) 0.2492 0.4996 0.6628 0.2121 0.0224 <0.0001 0.2193 0.6220
3(n=316) <0.0001 0.1538 0.2625 0.0473 0.0007 <0.0001 0.1484 0.2850
4(n=485) 0.0009 0.0274 0.0220 0.1588 <0.0001 <0.0001 0.0436 0.1190
5(n=350) 0.0026 0.0213 0.0232 0.0190 <0.0001 0.0010 0.0383 0.0406
6(n=260) 0.0735 0.1568 0.0063 0.0058 <0.0001 0.0290 0.0132 0.0105

670
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ESTLANDER ET AL.
ing ow h.Manyanimal axa,suchasbi dsingene al,ha eas ongin-
aspeci ic endency owa dla ge bodysizesa highe la i udesandin
coole en i onmen s(Ash on,2002),incon as  omanyec o he ms
(Angille a,S eu y,&Sea s,2004).Co obo a ingou  esul s,Heibo
e al.(2005) oundmanyli e-his o y a iables,suchasleng ha age
andleng hinc emen  odec easeandagea ma u i y oinc easewi h
la i ude.Thisisa ibu ed o hela i udinalclinein empe a u eand
du a iono  heg owingseason.Alsosuppo ingou  esul s, heas-
ymp o icbodyleng hdidno simila lyco ela ewi hla i ude.Inou 
da a, heg ow ho pe chdec easedwhile hea e ageleng handage
inc easedalongla i ude,sugges inga g ea e longe i yo no he n
popula ions.La gesizecanbe he esul o g ea e longe i y,i mo -
ali yislowe enwi h ela i elyslowg ow h(Angille ae al.,2004).
Incoole clima esa highe la i udes, ishmayin es mo einsoma ic
g ow h o eachala ge sizea  heexpenseo gonadg ow h,sug-
ges inga ade-o be weenindi idualene gyalloca ions.Yea -class
s eng ho pe chpopula ionsa dis ibu ion limi is alsoknown o
behighlydependen on empe a u e(Hayden,Ha od,&Kahilainen,
2014;Tolonen,Lappalainen,&Pulliainen,2003) ha mayalsop omo e
subsequen g ow ho singleyea class ola gesizeinmul ispecies
communi ies.Ingene al,pe chpopula ionsconsis o la ge sizedindi-
idualsinhighe la i udes(Jeppesene al.,2010),sugges ing ha  he
popula ion-le elshi  opisci o ymaybemo e equen  haninlowe 
la i udeso me ely e lec slowe  empe a u e- ela edme aboliccos s
and hushighe longe i yinno h.Also,o he bio ic ac o s,no con-
side edhe e,suchasa ailable ood esou ces,in aspeci iccompe i-
ionandin e speci iccompe i iona ec g ow ho pe ch.Howe e ,
la i ude( empe a u e,du a iono  heg owingseason,p oduc i i y)
di ec lyandindi ec ly egula esse e alabio icandbio ic ac o sand
he e o epo en iallyalsoa ec  he ophicin e ac ionsbe weenspe-
cies(Jeppesene al.,2010).Acco dingly,ou  esul ssugges  ha in
addi ion osex-speci icsensi i i y oen i onmen , a ia ioninSSD
could esul  omsex-speci icdi e encesinlonge i y,ages uc u e,
o di e encesindie .Fu he  ieldandexpe imen als udiescombin-
ingsex-speci icdie a y,sizes uc u e,andli e-his o y ai da aa e
needed oassess hesepa e ns.
Somes udiesha esugges ed ha di e en  imingo ma u i ybe-
ween hesexesmaybe esponsible o  hele elo SSD exhibi ed
byaspecies(Fai bai n,1990;Gibbons&Lo ich,1990).Theses udies
imply ha ju enileg ow h a esbe ween hesexesa esimila ,and
heea lie ma u ingsex emainssmalle  han hela e ma u ingsex
(Badyae ,2002).In hiss udy,malesma u edea lie  han emales,a
pa e ncommonin ish,as emalesinc ease hei  ecundi ywi hsize,
bu  ep oduc i esuccessinmalesisno assize-dependen (S ea ns,
1992).Howe e ,Blanckenho ne al.(2007)sugges edinas udywi h
FIGURE2 P opo iono o e allg ow h
( o alleng hin e men )o  emale(open
ci cles)andmale(black iangles)pe chin
he i s yea (a)and i hyea (b)
0
10
20
30
40
50 60 63 69
(a)
0
5
10
15
50 60 63 69
(b)
P opo ion o o e all g ow h
La i ude (°N)
TABLE3 Agea ma u i y(±SD)a di e en la i udeses ima ed
acco ding oHeibo(2003)bylinea  eg essionand heco esponding
o alleng hs o  heseagesanalyzed omda a
La i ude (°N)
Age a ma u i y
(yea s)
Leng h a ma u i y (mm)
Males Females
50° 2±0.18 131±17 138±21
60° 3±0.21 126±21 154±24
63° 4±0.27 142±20 164±25
69° 5±0.18 180±38 190±41
TABLE4 S epwisemul iple eg essionmodel( ac o sincluded
when p<.05) o sexualsizedimo phism.Theonly ac o selec ed
wasla i ude
β p
La i ude 0.731 13.561 .0001
Longi ude −0.018 −0.142 .889
Al i ude −0.146 −1.614 .122
Lakesize −0.149 −1.466 .158
To alphospho us −0.214 −1.762 .093
FIGURE3 La i ude-speci icdeg eeo sexualsizedimo phism
inpe chpopula ions(SDI=−0.01×la i ude+0.731,R2=.84,
p<.0001)
0.0
0.1
0.2
0.3
45 50 55 60 65 70
SDI
La i ude (°N)
|
671
ESTLANDER ET AL.
insec s ha SSDismo elikely ela ed odi e en ialg ow h a esbe-
ween hesexes ha maybedi e en lycons ainedbyg ow hcondi-
ionswhena aining hei op imalbodysizesand hela ge sexshows
s onge  esponse oa educ ioninen i onmen alquali y.The esul s
o ou  esea chsuppo  hissugges ion,becausepe chshowedasex-
dependen di e enceinsizeand back-calcula edg ow hal eadya 
heju eniles age,as emalesappea ed oin es mo eing ow hin he
ea lyyea so li e.Fas e g owing isha ealsomo elikely oshi  o
pisci o y ha maybemo eimpo an  o  emalesbene i ingonla ge 
ma u i ysizemo e hanmales.Thiscouldbeanimpo an mechanism
ounde s andbimodalsizes uc u eo pe chpopula ionsaswellas
p ey ishcommuni ies,bu  emains obee alua edinexpe imen al
and ields udies.The e o e,wea gue ha g ow h a e, a he  han
imingo ma u i y,maybeamo esigni ican  ac o behindSSD a i-
a ioninpe ch.I mus beno ed,howe e , ha i isdi icul  o ank
hese wo ac o sino de o impo ance,as heseli e-his o y ai sa e
highlyco ela ed(S ea ns,1992).
The eisalinea  ela ionshipwi hla i udeand empe a u e,and
ising empe a u eaccele a esg ow handea lie ma u i y(Be igan
&Cha no ,1994;Heiboe al.,2005),demons a edalsoin hiss udy,
as hema u a ionleng handagea ma u i yinc easedwi hla i ude
inbo h sexes.Typically,delayedma u a ionp o idesa bene i ,be-
cause ecundi yinc easeswi hbodysize(Ro ,2002;S ea ns,1992).
Acco ding oHeiboe al.(2005), hemaximum ep oduc i eli espan,
ha is,highe longe i yinc easeswi hla i udeinpe ch,bu  ep oduc-
i ein es men (measu edas ela i egonadmass)ineachspawning
seasondec easeswi hla i ude.Suchli e-his o ys a egyisbene icial,
i mo ali yislow, ha is, ep oduc i eli espano bo hsexesislong.
Simila  indings a e sugges ed also in coho salmon (Onco hynchus
kisu ch)as heeggnumbe inc eases,bu  heindi idualeggsizeand
he o aleggbiomassdec easewi hla i ude,and hus,a  hepopula-
ionle el, hegame ice o maybecons an wi hla i ude(Tama e&
Maekawa,2006).
O e all, he egula iono SSDisacomplica edissueandwidely
accep edecological ulessuchasRensch’sandBe gmann’s ulesde-
sc ibing hepa e nsinbodysizea eno s aigh o wa dlyapplicable
in ishspecieswi h emale-biasedSSD.Fo ins ance,e eni  ecundi y
selec ionwouldbe heul ima ecausebehind heSSDo  ish,se e al
en i onmen al ac o smigh  egula e hemagni udeo SSD,suchas
la i ude ha po en ially egula esacomplexmixo en i onmen aland
ecological ac o s.Mo eo e ,sensi i i y o hese ac o smay a ybe-
weensexes.Inaddi ion,i isdi icul  odis inguishwhe he pheno-
ypicchangesing ow ho size/ages uc u ealongala i udeg adien 
a ea esul o adap i ee olu iono pheno ypicplas ici yo amix u e
o bo h(e.g.,Kupa inen&Me ilä,2007),and hus,mo e esea chis
needed,suchascommonga denexpe imen s, obe e unde s and
bo h he pheno ypic and gene ic ela ionships be ween SSD and
g ow h.Ou  esea chdemons a esla i udinalpopula ion-le el a i-
a ionin hemagni udeo SSDbasedong ow h a e,suppo ing he
p edic ionso p e iousexpe imen aland egionals udiesbyFon aine,
Ga deu ,Kes emon ,andGeo ges(1997),Ho ppilae al.(2011),and
Es lande e al.(2015),allsugges ing ha en i onmen al ac o slim-
i ingo e allg ow hmaydec ease hemagni udeo SSD.Thiss udy
alsohighligh s heimpo anceo sex-speci ic esponsedi e ences o
en i onmen al a iablesin egula ingpa e nso allome ybe ween
hesexesin ish.Ingene al,unde s anding hecausesbehindbody
size a ia ionispa icula lyimpo an in ishasi is ela ed o ecun-
di y and su i al. Ou  esul s o  g ow h and sexual ma u i y o  an
abundan  ishinEu opeanlakessugges  ha sexhasanimpo an  ole
inde e miningli e-his o y ai s,bu mayha eimplica ionsonindi-
idualme abolism,p eda o –p ey ela ionships,andsizes uc u ing
o  ishpopula ionsinlakes.Weconclude ha  ollow-ups udies om
indi idual oecosys emle elscalea eneeded oassesspo en ially
holis icconsequenceso sexualsizedimo phism.
ACKNOWLEDGMENTS
The s udy was inancially suppo ed by h ee-yea  esea ch g an s
om heUni e si yo Helsinki, heR.E ikSe lachiusFounda ion,and
heBe gs åde B o Se lachiusFounda ion.We hankallo  hepeople
whopa icipa edin ieldsamplingandlabo a o yanalyseso  ish.
CONFLICT OF INTEREST
Nonedecla ed.
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