Gene ics o Mic oen i onmen al Sensi i i y o Body
Weigh in Rainbow T ou (
Onco hynchus mykiss
)
Selec ed o Imp o ed G ow h
Ma i Janhunen
1
*, An i Kause
1
, Ha i Veh ila
¨inen
1
, O so Ja
¨ isalo
2
1MTT Ag i ood Resea ch Finland, Biome ical Gene ics, Jokioinen, Finland, 2Finnish Game and Fishe ies Resea ch Ins i u e, Laukaa, Finland
Abs ac
Mic oen i onmen al sensi i i y o a geno ype e e s o he abili y o bu e agains non-speci ic en i onmen al ac o s, and i
can be quan i ied by he amoun o esidual a ia ion in a ai exp essed by he geno ype’s o sp ing wi hin a
(mac o)en i onmen . Due o he high deg ee o polymo phism in beha io al, g ow h and li e-his o y ai s, bo h a med and
wild salmonids a e highly suscep ible o mic oen i onmen al a ia ion, ye he he i able basis o his cha ac e is ic emains
unknown. We es ima ed he gene ic (co) a iance o body weigh and i s esidual a ia ion in 2-yea -old ainbow ou
(Onco hynchus mykiss) using a mul igene a ional da a o 45,900 indi iduals om he Finnish na ional b eeding p og amme.
We also es ed whe he o no mic oen i onmen al sensi i i y has been changed as a co ela ed gene ic esponse when
gene ic imp o emen o g ow h has been p ac iced o e i e gene a ions. The animal model analysis e ealed he p esence
o gene ic he e ogenei y bo h in body weigh and i s esidual a ia ion. He i abili y o esidual a ia ion was ema kably
lowe (0.02) han ha o body weigh (0.35). Howe e , gene ic coe icien o a ia ion was no able in bo h body weigh
(14%) and i s esidual a ia ion (37%), sugges ing a subs an ial po en ial o selec ion esponses in bo h ai s. Fu he mo e,
a signi ican nega i e gene ic co ela ion (20.16) was ound be ween body weigh and i s esidual a ia ion, i.e., apidly
g owing geno ypes a e also mo e ole an o pe u ba ions in mic oen i onmen . The gene ic ends showed ha ish
g ow h was success ully inc eased by selec i e b eeding (an a e age o 6% pe gene a ion), whe eas no gene ic change
occu ed in esidual a ia ion du ing he same pe iod. The esul s imply ha gene ic imp o emen o body weigh does no
cause a concomi an inc ease in mic oen i onmen al sensi i i y. Fo comme cial p oduc ion, howe e , he e may be high
po en ial o simul aneously imp o e weigh gain and inc ease i s uni o mi y i bo h c i e ia a e included in a selec ion index.
Ci a ion: Janhunen M, Kause A, Veh ila
¨inen H, Ja
¨ isalo O (2012) Gene ics o Mic oen i onmen al Sensi i i y o Body Weigh in Rainbow T ou (Onco hynchus
mykiss) Selec ed o Imp o ed G ow h. PLoS ONE 7(6): e38766. doi:10.1371/jou nal.pone.0038766
Edi o : S ephen Moo e, Uni e si y o Queensland, Aus alia
Recei ed Feb ua y 21, 2012; Accep ed May 14, 2012; Published June 11, 2012
Copy igh : ß2012 Janhunen e al. This is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s
un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed.
Funding: MTT Ag i ood Resea ch Finland (u l: www.m . i). The unde s had no ole in s udy design, da a collec ion and analysis, decision o publish, o
p epa a ion o he manusc ip .
Compe ing In e es s: The au ho s ha e decla ed ha no compe ing in e es s exis .
* E-mail: [email p o ec ed]
In oduc ion
Ea ly phases o selec i e b eeding can gene a e apid gene ic
esponses in a med animals. This ypically in ol es gene ic
imp o emen o mean pe o mance in he di ec ion o selec ion.
I is well es ablished ha many concu en imp o emen s in
animal husband y, including nu i ion, housing and e e ina y
p ac ices, accompany he gene ic enhancemen in animal pe o -
mance. Addi ionally, ai he e ogenei y can e ol e o e ime, o
example ia inc eased o educed suscep ibili y o indi iduals o
a iable and unmeasu ed mic oen i onmen al ac o s. Unde -
s anding he gene ic basis o such concu en changes in
quan i a i e ai s e eals how selec ion in luences he abili y o
indi iduals o espond o unp edic ably luc ua ing en i onmen al
condi ions ia de elopmen al mechanisms, and helps us o explain
he pe sis ence o pheno ypic a iabili y wi hin popula ions.
Mic oen i onmen al sensi i i y e e s o an indi idual’s abili y
o be bu e ed agains local non-speci ic en i onmen al ac o s
(e.g., luc ua ing wea he , ligh condi ions and ood supply, and
compe i i e social in e ac ions) and sub le de elopmen al noise,
and i is conside ed synonymous o de elopmen al ins abili y [1–
3]. Mic oen i onmen al sensi i i y o a geno ype can be
quan i ied by he amoun o esidual a ia ion in a ai
exp essed by he geno ype’s o sp ing wi hin a (mac o-)en i on-
men he o sp ing sha e. In mode n quan i a i e gene ic analysis,
esidual a iance can be bes es ima ed using an animal model
which pa i ions a pheno ype o an indi idual in o i s addi i e
gene ic and esidual componen s, he la e being he pa le
unexplained by gene ics and sys ema ic ixed e ec s such as
gende , age and managemen ea men s [4,5]. In a m animal
husband y, inc eased esidual and hus pheno ypic a ia ion is
disad an ageous because i hampe s he e iciency o p oduc ion
h oughou he supply chain om p oduce s o consume s [6,7].
Mo eo e , la ge size a ia ion in ea ing g oups p omo es he
o ma ion o beha io al dominance hie a chies which educe
animal wel a e and ele a e mo ali y [8–10]. This can be pa ly
a oided by ac i e size so ing and g ouping o animals.
Cu en ly, he e is inc easing in e es o in es iga e o wha
ex en esidual a ia ion can be gene ically educed by animal
b eeding p og ammes.
Pe manen changes in mic oen i onmen al sensi i i y a e
possible only when he e is addi i e gene ic a ia ion o esidual
a ia ion. In o he wo ds, di e en geno ypes should p oduce
PLoS ONE | www.plosone.o g 1 June 2012 | Volume 7 | Issue 6 | e38766
di e en ly a iable p ogenies. The ecen e idence om bo h wild
and a med animals imply ha geno ypes indeed di e in hei
amoun o esidual a ia ion o ai s [11]. E en hough he i abili y
o esidual a ia ion is gene ally low, i can be exploi ed o inc ease
uni o mi y by di ec selec ion [12–16]. Fu he , i has been
sugges ed ha in ense di ec ional selec ion o a ai (mean) alue
can lead o inc eased esidual (and hus pheno ypic) a ia ion
because he ex eme indi iduals wi h a highe selec ion p obabili y
a e also he geno ypes passing down high a iabili y [14,17,18].
This would be wo isome because selec ion would make indi id-
uals mo e sensi i e o hei en i onmen . The coun e hypo hesis is
ha du ing adap a ion o an en i onmen , ei he in he wild o in
human-con olled condi ions o a med species, mic oen i on-
men al sensi i i y is dec eased due o he adap ion o a ocal
en i onmen [19,20].
P e ious wo k has concen a ed on e es ial e eb a es and
labo a o y model species, which g ea ly di e om aqua ic species,
and om salmonids in pa icula . Salmonids ha e a mul i ude o
cha ac e is ics ha make he gene ic analysis o mic oen i on-
men al sensi i i y in g ow h impo an . In aquacul u e p oduc ion,
new popula ions and species a e cons an ly in oduced in in ensi e
cap i e b eeding, p o iding an oppo uni y o in es iga e he
gene ic e ec s o a i icial selec ion (o domes ica ion p ocess [21])
on bo h he ai mean alue and i s unde lying a ia ion.
Fu he mo e, salmonids exhibi an ex ao dina y polymo phism
and di e si y in mo phological, beha io al and li e-his o y ai s,
including al e na i e g ow h, mig a ion and ep oduc ion s a e-
gies exp essed ac oss and wi hin single popula ions [22–25]. Some
o hese esponses a e adap i e esponses o he highly s ochas ic
na u al condi ions. Salmonids also display s ong dominance
hie a chies, especially wi hin a med popula ions, in which ew
indi iduals can de end ood esou ces, inc easing pheno ypic
a ia ion in g ow h [26–28]. Gi en ha ish as ec o he ms a e
pa icula ly sensi i e o a ying ambien condi ions ha can
in luence on ogene ic ajec o ies, indi idual di e ences in g ow h
a e mo e p onounced in ish compa ed o a med e es ial
animals. Fo example, in cul u ed salmonids, pheno ypic coe i-
cien o a ia ion (CV) o body weigh a ies be ween 20–40%
[29], whe eas in chicken and pigs i is a ound 10–15% [30–32].
Finally, an addi ional s eng h o using salmonids o s udy gene ic
a chi ec u e o mic oen i onmen al sensi i i y is ha he es ab-
lished b eeding p og ammes gene a e la ge numbe o amilies in
successi e gene a ions, and due o hei high ecundi y, high amily
sizes can be p oduced, bo h ac o s needed o an e ec i e gene ic
analysis o esidual a ia ion.
To in es iga e he inhe i ance o mic oen i onmen al sensi i i y
and i s gene ic esponses ac oss gene a ions when di ec ional
selec ion is pe o med o imp o ed g ow h, we analyzed
mul igene a ional pedig eed da a co e ing en yea classes and
46 546 indi iduals om he Finnish b eeding p og amme o
ainbow ou , Onco hynchus mykiss (Walbaum). We i s es ima ed
he p opo ion o gene ic a ia ion in esidual a ia ion o body
weigh in ish being main ained in he same loca ion. By p o iding
a common mac oen i onmen ac oss yea classes and by using he
animal model, we ensu ed ha esidual a ia ion can be ega ded
as mic oen i onmen al sensi i i y (o de elopmen al s abili y) ha
esul s om non-sys ema ic en i onmen al ac o s and in e nal
de elopmen al noise. Second, we es ima ed he gene ic co ela ion
be ween he addi i e gene ic e ec s o body weigh and i s
esidual a ia ion. Finally, by es ima ing gene ic ends ha
quan i y gene ic esponses ac oss mul iple gene a ions, we
in es iga ed he e ec s o selec i e b eeding o body weigh on
he gene ic change in mic oen i onmen al sensi i i y.
Me hods
E hics S a emen
All p ocedu es in ol ing animals we e app o ed by he animal
ca e commi ee o he Finnish Game and Fishe ies Resea ch
Ins i u e (FGFRI).
Da a Sou ce
The da a o igina ed om he Finnish na ional ainbow ou
b eeding p og amme main ained by he FGFRI and MTT
Ag i ood Resea ch Finland. The b eeding nucleus is held a he
Te o Fishe ies Resea ch and Aquacul u e s a ion in Cen al
Finland (63u19N, 26u399E).
The pheno ypic da a included 45 900 eco ds o body weigh
om indi iduals bo n du ing 1992–2002 and ea ed a he same
eshwa e nucleus s a ion. The ish ep esen ed eigh yea classes
and belonged o wo subpopula ions wi h ou successi e
gene a ions (Pop I and Pop IIa) [33,34]. Each yea class consis ed
o 94–270 ull-sib amilies es ablished om ma ings o 37–90 si es
wi h 92–270 dams. The subpopula ions sha e a common gene ic
base om which he ounding indi iduals we e sampled in 1989
o PopI and in 1990 o PopII. E en hough he base popula ion
was p eceded by a long- e m cul i a ion backg ound, only he
s udied gene a ions belong o a sys ema ic b eeding p og amme in
which in ensi e gene ic selec ion based on es ima ed b eeding
alues has been p ac iced. The pedig ee in o ma ion ex ended
o e he i e gene a ions and comp ised 46 546 indi iduals,
including he 364 base popula ion animals wi hou pheno ypic
obse a ions.
The gene a ion in e al o he s udy popula ion was 3–4 yea s.
Annual selec ion o b eeding candida es was made using a
mul i ai selec ion index wi h main emphasis on imp o ed g ow h
The selec ion index has consis ed o bes linea unbiased
p edic ions o b eeding alues o body weigh measu ed a he
age o 2 and 3 yea s (since 1992), ma u i y age (since 2001) [35],
and body shape, skin colo and i s spo iness (since 2001) [36].
Pa en al ish we e ma ed in sp ing using ei he nes ed pa e nal
hie a chical o pa ial ac o ial designs [33].
Full-sib egg ba ches we e incuba ed sepa a ely, and a he eyed-
egg s age, hey we e ans e ed o one o wo 150-li e indoo amily
anks. Ha ching o eggs occu ed in June. Du ing he ollowing
win e , a e six mon hs o g owing in he amily anks, equal amoun
o inge lings (o 50–100 g body weigh ) om each amily ank we e
haphaza dly sampled and indi idually agged wi h passi e in eg a -
ed ansponde s (T o an, L d., Ulm, Ge many) and hen ans e ed
o a low- h ough ea h-bo omed aceway a he Te o s a ion. The
ish we e ed wi h comme cial d y eed. In Finland, yea is highly
seasonal and he e ec i e g owing season las s om ea ly May o la e
Oc obe .
A e he second g owing season, he wo-yea -old ish we e
indi idually weighed o he nea es 1 g (mean 10206315 (SD) g, n
= 45 900). The numbe o indi iduals wi hin each yea class
anged be ween 2 518–10 753. The p opo ion o sexually
ma u ed (2+) males in he en i e da a-se was 14.9%, whe eas no
ma u e emales we e ound.
To imp o e he eliabili y o gene ic pa ame e s o esidual
a ia ion, only si e amilies wi h a leas 35 o sp ing (n= 457 si es)
we e selec ed o he analysis. La ge amily sizes a e needed o
ob ain accu a e and unbiased gene ic pa ame e s and es ima ed
b eeding alues (EBVs) o esidual a ia ion [14].
Gene ic Analysis
The es ima ion o gene ic pa ame e s and gene ic ends was
conduc ed using a bi a ia e animal model [31]. The ASReml 3.0
Residual Va ia ion in Rainbow T ou Body Weigh
PLoS ONE | www.plosone.o g 2 June 2012 | Volume 7 | Issue 6 | e38766
so wa e applying es ic ed maximum likelihood (REML) was
used [37]. The i s ai was body weigh o which a linea mixed
‘mean model’ was i ed:
yijk~mzyea jz an kkzAizeijk ð1Þ
whe e yijk is body weigh o an indi idual i,
m
is he o e all
popula ion mean, yea jis he ixed e ec o bi h yea (j= 8 yea s),
an kkis he andom in e ac ion e ec be ween bi h yea and
common en i onmen sha ed by ull-sibs be o e agging (k=
amily an k6yea numbe ), Aiis he andom gene ic animal
e ec wi h a pedig ee (i= numbe o animals), and eijk is he
esidual e o e m wi h sepa a e a iance s2
es o each si e amily
s . The common en i onmen e ec is modeled wi hou he
pedig ee in o ma ion. The alues o Akaike’s In o ma ion
C i e ia (AIC) [38] and Bayesian In o ma ion C i e ia (BIC)
[39] we e lowe o he model wi h he e ogeneous esidual
a iance s uc u e, sugges ing a be e i o he da a compa ed o
he model wi h homogeneous esidual a iance (AIC: 539554 and
542160; BIC: 541235 and 542171, espec i ely).
The second ai was mic oen i onmen al sensi i i y which was
quan i ied by he log- ans o med squa ed esidual alues, ln (e2
ijk),
ob ained om he mean model (1) and used as new obse a ions in
he ‘ a iance model’. Log- ans o med squa ed esidual alues
quan i y he con ibu ion o each indi idual o popula ion’s
esidual a ia ion [15,31,32,40]. In con as o si e-dam models,
he esiduals o an animal model include only unexplained
en i onmen al and de elopmen al noise, and hey a e no
con ounded by he addi i e gene ic Mendelian sampling e m.
The animal ‘ a iance model’ was:
ln (e2
ijk)~mzyea jzA esize esij ð2Þ
whe e A esiis he gene ic e ec o animal i o ln (e2
ijk)and e esij is
he andom esidual e ec . Fo he andom e ec s o ln (e2
ijk), he
assump ions we e A es*N(0, As2
A es )and e es*N(0, Is2
e es ),
whe e Ais he addi i e gene ic ela ionship ma ix wi h addi i e
gene ic a iance s2
A es and Iis he iden i y ma ix wi h
homogeneous esidual a iance s2
e es :The andom e ec o
common en i onmen 6bi h yea was omi ed om he a iance
model because i s a iance explained less han 2% o he o al
pheno ypic a iance and i did no signi ican ly di e om ze o.
Because he esiduals o he model 1 a e used as an inpu
a iable o he model 2, he model o he mean and he esidual
a ia ion was i e a i ely sol ed by conduc ing 30 consecu i e
bi a ia e analyses. A each i e a i e ound, ln (e2
ijk) o he
a iance model we e upda ed wi h esiduals om he p e ious
ound’s mean model. The esiduals eijk and e esijk we e assumed o
ollow a bi a ia e no mal dis ibu ion and be unco ela ed (i.e.,
hei esidual co a iance was se o ze o). The con e gence c i e ia
wi hin sepa a e uns we e ul illed when he REML log-likelihood
changed less han 0.002 6i e a ion numbe and he indi idual
a iance pa ame e es ima es changed less han 1% be ween
successi e i e a ions [37].
Calcula ion o Gene ic Pa ame e s and Gene ic T ends
He i abili y o weigh mean was calcula ed as h2~s2
A=s2
Pand
he common en i onmen e ec a io as c2~s2
an k=s2
Pusing he
a iance componen s om model 1. He e s2
P~s2
an kzs2
Azs2
e,
whe e s2
eis he a e age esidual a iance o si e amilies. In
addi ion o common en i onmen e ec s o ull sibs, s2
an kmay
include pa s o non-addi i e gene ic and ma e nal a iance.
Gene ic coe icien o a ia ion was calcula ed as GCV~sA=m,
whe e
m
is he pheno ypic mean o he popula ion. GCV desc ibes
he p opensi y o he ai o espond o selec ion, ha is, i s
e ol abili y [41].
He i abili y o esidual a ia ion was calcula ed as
h2
~s2
AV=(2s4
Pz3s2
A ), whe e s2
A is he ans o med addi i e
gene ic a iance o esidual a ia ion om model 2 and s2
Pis he
pheno ypic a iance o body weigh ob ained om model 1 [14].
The gene ic a iance s2
A was calcula ed as s2
A ~h2
es2(s2
e)2,whe e
h2
es~s2
A es =(s2
A es zs2
e es )is he he i abili y o ln (e2
ijk)and s2
eis he
a e age esidual a iance ob ained om model 1. Gene ic
coe icien o a ia ion o esidual a ia ion was calcula ed as:
GCVE~sA =s2
e:An es ima e o gene ic co ela ion be ween he
addi i e gene ic e ec s o body weigh and i s esidual a iance
was ob ained om he bi a ia e analysis whe e di ec es ima ion o
co- a iance be ween he wo ai s is possible.
The app oxima e s anda d e o s o es ima ed a iance
componen s and a iance a ios we e calcula ed using ASReml.
The s anda d e o o h2
was app oxima ed acco ding o Mulde
e al. [31].
REML log-likelihood alues and he pa ame e es ima es o
body weigh we e ound o emain ela i ely s able ac oss he 30
i e a i e ounds, whe eas s2
A es oscilla ed. The e o e, he esul s
om bi a ia e analysis a e p esen ed as a e ages o all ASReml
uns (n= 30 ounds). The obse ed oscilla ion is inhe en o he
s a is ical model used and is mainly due o an in e play be ween
Ai,A esiand he esidual eijk:An inc ease in Aicauses a dec ease
in he esidual and he eby lowe s A esi(and ice e sa).
To in es iga e whe he o no gene ic changes in mean body
weigh and i s mi c oen i onmen al sensi i i y occu ed du ing
selec i e b eeding, gene ic ends we e de e mined o bo h ai s
and o bo h subpopula ions sepa a ely. The gene ic ends we e
ob ained by plo ing he a e age es ima ed b eeding alues (i.e.,
he p edic ed gene ic le els o yijk and ln (e2
ijk)ob ained om
indi iduals’ a e ages ac oss he 30 i e a i e ounds) agains he
bi h yea o ish.
Resul s
Gene ic Va ia ion
He i abili y o body weigh was mode a e (0.35), whe eas he
common en i onmen a io was low (0.05) (Table 1). Gene ic
coe icien o a ia ion o body weigh was sligh (0.14).
He i abili y es ima e o esidual a ia ion was low (0.02), hough
i was g ea e han i s s anda d e o (Table 2). Ye , he
mode a ely high gene ic coe icien o a iance o esidual
a ia ion (GCV
E
= 0.37) sugges s ha he e is no able gene ic
po en ial in mic oen i onmen al sensi i i y o body weigh .
Gene ic Co ela ion be ween Body Weigh and i s
Residual Va ia ion
The e was a sligh bu signi ican nega i e gene ic co ela ion
be ween body weigh and i s esidual a ia ion
( G=20.15760.039 (S.E.)), indica ing ha high body weigh
was gene ically associa ed wi h dec eased mic oen i onmen al
sensi i i y.
Gene ic T ends
Body weigh showed a clea gene ic imp o emen du ing he
s udy pe iod. O e he ou gene a ions o selec ion, he
Residual Va ia ion in Rainbow T ou Body Weigh
PLoS ONE | www.plosone.o g 3 June 2012 | Volume 7 | Issue 6 | e38766
cumula i e gene ic gains in he wo sub-popula ions we e 199 g o
208 g, co esponding o an a e age o 0.83 inc ease in pheno ypic
s anda d de ia ion o 5.5% pe yea (Fig. 1a). In con as , mean
es ima ed b eeding alues o mic oen i onmen al sensi i i y
emained s able ac oss he yea classes (Fig. 1b).
Discussion
Low He i abili y bu Mode a e E ol abili y o
Mic oen i onmen al Sensi i i y
We ound a low 0.02 he i abili y es ima e o esidual a ia ion
o body weigh (i.e., mic oen i onmen al sensi i i y) in 2-yea -old
ainbow ou . This is in ma ked con as wi h he mode a e
he i abili y o 0.35 o body weigh . The low he i abili y es ima e
o mic oen i onmen al sensi i i y is somewha su p ising as la ge
wi hin- and be ween- amily a ia ion in ish g ow h is c ea ed by
mul iple ac o s, some o hem p esumably exhibi ing subs an ial
gene ic a ia ion. Howe e , he no able gene ic coe icien o
a ia ion (37%, when gene ic a ia ion o esidual a iance is
scaled by a e age esidual a iance) indica es he p esence o
subs an ial addi i e gene ic a ia ion o mic oen i onmen al
sensi i i y. Rega ding mos li e-his o y ai s, he low he i abili ies
ye pa adoxically high e ol abili y a e a ibu ed o he high
esidual a ia ion accumula ing om he a iable unde lying
physiological and beha io al ai s [41,42]. Simila ly, body weigh
and i s a ia ion can be in luenced by many unde lying
componen ai s such as eeding beha io , eed u iliza ion and
me abolism [43].
The e a e se e al ac o s ha can main ain gene ic a ia ion in
mic oen i onmen al sensi i i y in he popula ion unde s udy.
Fi s , high ini ial g ow h a es and ene gy esou ces a e ela ed o
inc eased p obabili y o ea ly ma u a ion in salmonids [44,45].
Likewise, in ainbow ou , apid g ow h is gene ically and
pheno ypically co ela ed o ea ly ma u i y age [35,46,47]. In
ou popula ion, male ish p ima ily ma u e a ages o 2 o 3 yea s.
Ma u i y age in males has a mode a e he i abili y o 0.23–0.34,
and hus he e a e amily di e ences in he equency o ma u ing
indi iduals [33,35]. This alone may c ea e gene ic a ia ion in
mic oen i onmen al sensi i i y: high esidual a ia ion would be
ound in amilies wi h bo h ea ly and la e ma u ing indi iduals,
and low esidual a ia ion in amilies wi h ei he only ea ly o only
la e ma u ing indi iduals. Acco dingly, i was logical no o include
ma u a ion as a ixed ac o in he s a is ical model because sexual
de elopmen i sel cap u es pa o he wi hin- amily a ia ion we
we e in e es ed in. Second, ollowing he o me easoning, he
gene ic a ia ion obse ed o esis ance and/o ole ance o
pa asi e-media ed ca a ac (Diplos omum spp.) in ou popula ion
may c ea e gene ic a ia ion in mic oen i onmen al sensi i i y.
Some amilies emain unin ec ed while o he s ha e bo h in ec ed
and unin ec ed indi iduals, and he in ec ed indi iduals exhibi
educed g ow h [48]. Thi d, social in e ac ions associa ed wi h
beha io and g ow h di e ences ha e also been ound o c ea e
addi ional gene ic a ia ion in chicken and pigs [49,50], and
p esumably in ish as well [51]. A la ge p opo ion o he gene ic
a ia ion unde lying socially a ec ed ai s emains hidden, i.e., is
no accoun ed o by he di ec he i abili y es ima es, and can hus
only be e ealed by unexplained esidual a ia ion. Las , i is
impo an o ecall ha e en hough he gene ic cha ac e is ics o
a med ish popula ions a e in luenced by li e his o ies o igina ing
om hei wild ances o s, he esul s om a gene ic analysis o
a med popula ions canno be ex apola ed back o wild popula-
ions [52]. Ne e heless, he es ima es o gene ic pa ame e s
ob ained om a med popula ions help us o unde s and
biologically meaning ul phenomena and also ad ance gene al
knowledge o he ac o s unde lying pheno ypic a ia ion in
quan i a i e ai s [53].
Al hough ainbow ou , among o he salmonids, possess a
capaci y o conside able g ow h and li e-his o y s a egy a ia ion
bo h ac oss and wi hin amilies [33,35,54], he obse ed he i abili y
es ima e o esidual a ia ion in body weigh is o simila low
magni ude ha has been epo ed o less a iable e es ial animals
[11,14]. Co espondingly, GCV
E
was in he ange o hose ound in
chickens, mice, pigs and abbi s (25–50%) [11]. Fluc ua ing
asymme y, he deg ee o andom non-di ec ional de ia ions
be ween mo phological cha ac e is ics measu ed om le and igh
hand side o indi iduals, is an al e na i e measu e o de elopmen al
ins abili y. In acco dance wi h he o iginal idea by Le ne [55],
inc eased he e ozygosi y has been ound o educe luc ua ing
asymme y in bila e al ai s o bo h wild and a med ainbow ou
[56,57]. Howe e , he es ima ed low he i abili y o luc ua ing
asymme y led he au ho s o conclude ha dominance e ec s ha e a
majo con ibu ion o he con ol o de elopmen al s abili y [58].
De elopmen al ins abili y is o en assumed o be selec i ely
disad an ageous due o he inc eased isk o d i om he
pheno ypic op imum [3,59,60], bu empi ical suppo o his iew
is la gely inconclusi e [61]. I is p obable ha in some cases, such as
he mo phological ai s o plan s, selec ion a o s inc eased
sensi i i y as a be -hedging s a egy [62].
Table 1. Es ima es o a iance componen s and a iance
a ios (6app oxima e s anda d e o s) o body weigh .
Pa ame e
a
Es ima e
s2
A20 888 (1515)
s2
ank 3 089 (286)
s2
e35 674 (7444)
s2
P59 652 (7439)
h
2
0.350 (0.051)
c
2
0.052 (0.009)
GCV 0.142
a
addi i e gene ic a iance; s2
ank common en i onmen a iance; s2
e he a e age
esidual a iance o si e amilies; s2
Ppheno ypic a iance; h2– he i abili y,
h2~s2
A=s2
P;c2– common en i onmen e ec a io, c2~s2
ank=s2
P;GCV–
coe icien o gene ic a ia ion, GCV~sA=m.
doi:10.1371/jou nal.pone.0038766. 001
Table 2. Es ima ed a iance componen s and a iance a ios
(6app oxima e s anda d e o s) o mic oen i onmen al
sensi i i y o body weigh .
Pa ame e
a
Es ima e
s2
A es 0.374 (0.028)
s2
A 1.81 E +08
h2
0.024 (0.006)
GCV
E
0.376
a
addi i e gene ic a iance in ln(e
2
) (model 2);
s2
A – ans o med gene ic a iance in he quan i a i e gene ic model o
gene ic he e ogenei y o esidual a ia ion [13], s2
A ~h2
es2(s2
e)2;h2
–
he i abili y, h2
~s2
AV=(2s4
Pz3s2
A );
GCVE– gene ic coe icien o a ia ion, GCVE~sA =s2
e.
doi:10.1371/jou nal.pone.0038766. 002
Residual Va ia ion in Rainbow T ou Body Weigh
PLoS ONE | www.plosone.o g 4 June 2012 | Volume 7 | Issue 6 | e38766
I is possible ha simila o li e-his o y ai s [63–66], de elop-
men al s abili y is inhe en ly an impo an i ness co ela e, and he
s ong di ec ional selec ion du ing he long his o y o animals has led
o i s low he i abili y [58]. Meanwhile, many unde lying en i on-
men al and gene ic ac o s a ec ing mic oen i onmen al sensi i i y
e ain i s gene ic coe icien o a ia ion a a mode a e le el.
Ne e heless, u he analyses a e needed o es whe he he gene ic
pa ame e s show simila alues in wild ish popula ions o when ish
Figu e 1. Gene ic changes in mean and esidual a ia ion o body weigh . A e age gene ic changes o A) body weigh mean and B) i s
mic oen i onmen al sensi i i y in wo subpopula ions (black and g ey box) o ainbow ou . The a e ages a e gi en in he uni s o pheno ypic
s anda d de ia ion (s
P
).
doi:10.1371/jou nal.pone.0038766.g001
Residual Va ia ion in Rainbow T ou Body Weigh
PLoS ONE | www.plosone.o g 5 June 2012 | Volume 7 | Issue 6 | e38766

popula ions a e in hei i s gene a ions o domes ica ion. The
me hods de eloped by animal b eede s and also used he e [31,32]
can be applied o wild popula ions when pedig ee in o ma ion is
es ablished using molecula gene ic ma ke s.
Di ec and Co ela ed Responses o Selec ion in
Mic oen i onmen al Sensi i i y
The low he i abili y es ima e obse ed he e does no necessa ily
indica e ha mic oen i onmen al sensi i i y would be weakly
esponsi e o selec ion. He i abili y, he a io o addi i e gene ic
a iance o pheno ypic a iance, is one p edic o o gene ic
po en ial o selec ion esponses, hough in his con ex , gene ic
coe icien o a ia ion p o ides a mo e easonable measu e o
e ol abili y, simila o GCV o ai means [41,67]. In ou s udy,
GCV
E
was o e wo imes highe han GCV o body weigh ,
sugges ing a good oppo uni y o ob ain educ ion in andom
en i onmen al a ia ion by selec ion.
Some selec ion expe imen s and b eeding p og ammes ha e
ob ained conside able gene ic esponses in ai s wi h low he i abil-
i y (e.g., de elopmen al s abili y in D osophila [68,69]; pigle su i al
[70]), suppo ing he idea ha also he amoun o esidual a ia ion
can be modi ied by selec ion. Simila ly, esidual a ia ion is
expec ed o be educed by 10% a e one gene a ion o selec ion
when i is included in a selec ion index along wi h he pheno ypic
ai alue [71]. To e ec i ely b eed o a ai wi h a low he i abili y,
pheno ypic eco ds om a la ge numbe o ela i es a e equi ed.
Con olled ma ings and la ge amily sizes inhe en o ainbow ou
and many o he aquacul u e species enhance he es ima ion o
b eeding alues wi h mode a e accu acy [14,72].
To ou knowledge, his s udy is he i s mul igene a ional
b eeding expe imen on aqua ic o ganisms o assess he co ela ed
gene ic e ec o s ong di ec ional selec ion on mic oen i onmen-
al sensi i i y o a ai . The gene ic co ela ion be ween body
weigh and i s esidual a ia ion was nega i e, implying ha a high
ai alue was linked o a sligh ly educed mic oen i onmen al
sensi i i y. This combined wi h he low he i abili y o esidual
a ia ion p edic s only a weak dec easing mic oen i onmen al
sensi i i y ac oss successi e gene a ions in esponse o selec ion o
apid g ow h. Howe e , he gene ic end o mic oen i onmen al
sensi i i y emained s able o sligh ly ele a ed o e he cou se o
he selec ion pe iod, while body weigh mean displayed a 6%
gene ic inc ease pe gene a ion. These esul s oge he indica e
ha gene ic imp o emen o body weigh does no make ainbow
ou mo e sensi i e o mic oen i onmen al pe u ba ions. This is
impo an animal wel a e issue, because inc ease in size he e o-
genei y would lead o se ious challenges in animal husband y.
In ense mass selec ion based on indi iduals’ own pheno ype is
expec ed o inc ease pheno ypic a ia ion wi hin a popula ion
e en when he e is no addi i e gene ic co ela ion be ween ai
and i s esidual a ia ion [14,18]. Mo eo e , s udies on salmonid
ish sugges ha selec ion o apid g ow h may indi ec ly selec o
compe i i e abili y and agg essi eness, hus inc easing he
likelihood o inc eased size a ia ion in a med ish du ing he
b eeding p ocess [73–76]. The obse ed pa e ns in gene ic ends
do no con o m o hese assump ions. Re e ing o he o me
p oposi ion, howe e , a mul i ai selec ion me hod in ou s udy
popula ion was no only based on he pheno ypic in o ma ion o
an indi idual i sel bu also he pe o mance o i s all ela i es was
aken in o accoun . This makes he p edic ions conce ning
esponses in en i onmen al a ia ion mo e di icul . Ne e heless,
he nega i e gene ic co ela ion be ween he body weigh and i s
mic oen i onmen al sensi i i y could be expec ed o coun e bal-
ance, o some ex en , he a e o inc ease in g ow h a ia ion due
o scale e ec s. P e ious s udies on e es ial animals ha e shown
ha he gene ic co ela ion be ween quan i a i e ai s and hei
esidual a ia ions can a y om nega i e o posi i e, depending
on he species and ai analyzed [31,40,77–79]. Simila inconsis-
en esul s ha e been ound in selec ion expe imen s. Fo
example, Iba´n˜ez-Esc iche e al. [16] demons a ed a dec ease in
pheno ypic CV o body weigh ai s in mice selec ed o inc eased
g ow h. In con as , long- e m selec ion expe imen s on D osophila
ui ly showed ha pheno ypic a ia ion can be subs an ially
highe in he lines selec ed o high and low abdominal b is le
numbe ela i e o he unselec ed base popula ion [80,81].
In conclusion, he e ogenei y o esidual a ia ion in ainbow
ou g ow h was ound o be pa ly unde gene ic con ol. This
implies he possibili y o selec ion o a o geno ypes wi h low
a iabili y when cons ancy ac oss mic oen i onmen al condi ions
is impo an . The nega i e gene ic ela ionship be ween body
weigh and i s mic oen i onmen al sensi i i y p esumably acili-
a es imp o ing weigh gain and simul aneously inc easing i s
uni o mi y/ obus ness i bo h objec i es a e inco po a ed in o a
selec ion index. In addi ion, inc easing he g ow h po en ial o ish
does no seem o cause a concomi an change in he ai ’s
mic oen i onmen al sensi i i y.
Acknowledgmen s
We exp ess ou g a i ude o he s a a he Te o Fishe ies Resea ch and
Aquacul u e s a ion o he solid da a collec ion and managing he ish.
Au ho Con ibu ions
Analyzed he da a: MJ. Mainly w o e he manusc ip : MJ. Took pa in
da a analysis and w i ing: AK. Took pa in w i ing he manusc ip : HV.
Con ibu ed ma e ials: OJ. Responsible o he main enance o he
expe imen : OJ.
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