Janhunen e al. Gene Sel E ol (2016) 48:94
DOI 10.1186/s12711-016-0272-3
RESEARCH ARTICLE
The mal sensi i i y o g ow h indica es
he i able a ia ion in1-yea -old ainbow ou
(Onco hynchus mykiss)
Ma i Janhunen1*, Juha Koskela2, Nguyễn Hữu Ninh3, Ha i Veh iläinen1, Heikki Koskinen4, An i Nousiainen4
and Ngô Phú Thỏa5
Abs ac
Backg ound: Rainbow ou is an impo an aquacul u e species, which has a wo ldwide dis ibu ion ac oss a ious
p oduc ion en i onmen s. The di e se loca ions o ou a ms in ol e ema kable a ia ion in en i onmen al ac o s such
as wa e empe a u e, which is o majo impo ance o he pe o mance o ish. Thus, obus ish ha could h i e unde
di e en and subop imal he mal condi ions is a desi able goal o ou b eeding. Using a spli - amily expe imen al
design (40 ull-/hal -sib g oups) o a ainbow ou popula ion de i ed om he Finnish na ional b eeding p og am, we
s udied how wo di e en ea ing empe a u es (14 and 20 °C) a ec eed in ake, g ow h a e and eed con e sion a io
in 1-yea -old ish. Fu he mo e, we quan i ied he addi i e gene ic (co-) a ia ion o daily g ow h coe icien (DGC) and i s
he mal sensi i i y (TS), de ined as he slope o he g ow h eac ion no m be ween he wo empe a u es.
Resul s: The ish showed consis en ly lowe eed in ake, as e g ow h and be e eed con e sion a io a he lowe
empe a u e. He i abili y o TS o DGC was mode a e (
h2
TS
=
0.24
). The co-he i abili y pa ame e de i ed om selec ion
index heo y, which desc ibes he he i able a iance o TS, was nega i e when he in e cep was placed a he lowe
empe a u e (−0.28). This esul ed in mode a e accu acy o selec ion. A he highe empe a u e, co-he i abili y o TS
was posi i e (0.20). The gene ic co ela ion be ween DGC and i s TS was s ongly nega i e (−0.64) when he in e cep
was a he lowe empe a u e and posi i e (0.38) bu no signi ican ly di e en om ze o a he highe empe a u e.
Conclusions: The conside able amoun o gene ic a ia ion in TS o g ow h indica es a po en ial o selec ion
esponse and hus o a ge ed gene ic imp o emen in TS. The nega i e gene ic co ela ion be ween DGC and i s
TS sugges s ha selec ion o high g ow h a e a he lowe empe a u e will esul in mo e empe a u e-sensi i e
ish. Ins ead, he co ela ed esponse o TS is less p onounced i he selec ion o a highe DGC occu ed a he highe
empe a u e. I seems possible o con ol he co ela ed gene ic change o TS while selec ing o as g ow h ac oss
en i onmen s, especially i measu emen s om bo h en i onmen s a e a ailable and b eeding alues o eac ion
no m slope a e di ec ly included in he selec ion index.
© The Au ho (s) 2016. This a icle is dis ibu ed unde he e ms o he C ea i e Commons A ibu ion 4.0 In e na ional License
(h p://c ea i ecommons.o g/licenses/by/4.0/), which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium,
p o ided you gi e app op ia e c edi o he o iginal au ho (s) and he sou ce, p o ide a link o he C ea i e Commons license,
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publicdomain/ze o/1.0/) applies o he da a made a ailable in his a icle, unless o he wise s a ed.
Backg ound
Di e en geno ypes, which a e ypically e e ed o as
sib-g oups, s ains o popula ions, may di e in hei
a e age pe o mance esponse o en i onmen al a i-
ables. In wild popula ions, an o ganism’s abili y o mod-
i y i s pheno ype in esponse o en i onmen al changes
( e med pheno ypic plas ici y) can i sel be an adap i e
li e-his o y ai , which is subjec o na u al selec ion
[1–4]. Pheno ypic plas ici y is conside ed synonymous o
mac o-en i onmen al sensi i i y, which is a mo e com-
monly used e m in he animal b eeding con ex [5]. Fo
animal b eede s, mac o-en i onmen al sensi i i y is an
impo an aspec due o i s associa ion wi h he animals’
pe o mance ac oss p oduc ion en i onmen s, and wi h
hei obus ness (s abili y) and wel a e [6–9].
Fo any measu able pheno ypic ai , he mac o-en i-
onmen al sensi i i y o a geno ype can be illus a ed as
Open Access
G
ene ics
S
elec ion
E olu ion
*Co espondence: [email p o ec ed]
1 Biome ical Gene ics, Na u al Resou ces Ins i u e Finland (Luke), Mylly ie
1, 31600 Jokioinen, Finland
Full lis o au ho in o ma ion is a ailable a he end o he a icle
Page 2 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
he esponse unc ion wi h en i onmen al change [10].
Assuming a linea eac ion no m, he deg ee o sensi-
i i y o a geno ype can be quan i ied by he eg ession
slope o a geno ype’s pe o mance ac oss an en i onmen-
al g adien [11, 12]. The exis ence o mac o-en i onmen-
al sensi i i y o a gi en ai is indica ed by slopes ha
de ia e om ze o, whe eas la eac ion no ms ac oss
he en i onmen al g adien axis e lec s abili y o he
ai . Since he eac ion no ms also depic he ex en o
e- anking among geno ypes and he change in addi i e
gene ic a iance wi h he en i onmen (i.e., wo o ms o
geno ype×en i onmen in e ac ion) hey can p o ide
in o ma ion abou he capaci y o popula ions and spe-
cies o adap o en i onmen al a iabili y [13].
The ainbow ou , Onco hynchus mykiss (Walbaum), is
an example o a globally impo an aquacul u e species,
which is dis ibu ed ac oss a ious p oduc ion en i on-
men s and sys ems, which ange om o sho e ne cages o
land-based e-ci cula ion acili ies. The di e se geog aphi-
cal loca ions o ainbow ou a ms may in ol e consid-
e able a ia ion in many abio ic (e.g., wa e empe a u e,
salini y, and pho ope iod) and bio ic (quali y o eed, pa h-
ogens and pa asi es) ac o s, which a e o majo impo -
ance o he pe o mance o ish. High g ow h capaci y
may be conside ed wo ldwide as he single mos economi-
cally impo an ai o be imp o ed by selec i e b eeding
[14], bu he capaci y o ish o exp ess he selec ed g ow h
po en ial unde a iable o subop imal en i onmen al con-
di ions may be cons ained. The e o e, a mo e obus ish
ma e ial wi h s abile g ow h would be an eligible p oduc
o b eeding unde a iable en i onmen al condi ions.
Being na i e o cool, empe a e egions o he no he n
hemisphe e, he ainbow ou , like all o he salmonids, is
adap ed o ela i ely low wa e empe a u es [15, 16]. S a-
bili y o g ow h is o special impo ance in ou a ming
a eas, whe e ea ing empe a u es emain cons an ly high
o whe e s ong seasonal wa ming occu s. Fu he mo e,
due o global wa ming, i is likely ha he e will be an
inc easing demand in he ish a ming sec o o popula-
ions o mo e hea - ole an ou in he u u e. To assess
whe he he mal sensi i i y (TS) o g ow h has he po en-
ial o be changed by selec ion, an es ima e o he addi-
i e gene ic componen in he slopes o eac ion no ms
is needed. The exis ence o gene ic a ia ion in g ow h
esponses as he empe a u e changes would enable he
de elopmen o mo e empe a u e- ole an o locally-
adap ed popula ions o di e en he mal condi ions.
In his s udy, we i s in es iga ed a a gene al (popula-
ion) le el how wo di e en ea ing empe a u es (14°C,
namely ‘low’, and 20 °C, namely ‘high’) in luence eed
in ake, g ow h and eed con e sion a io in 1-yea -old
ainbow ou . Second, by using a spli - amily design o
he expe imen , we quan i ied he addi i e gene ic (co-)
a ia ion o g ow h a e (daily g ow h coe icien , DGC)
and i s TS, he la e ai being de ined as he slope o he
eac ion no m be ween he wo empe a u e condi ions.
Me hods
S udy ma e ial
The ish used in his s udy we e de i ed om he Finnish
na ional b eeding p og am ha is main ained a he Te o
ish a m (b eeding nucleus) by he Na u al Resou ce
Ins i u e Finland (Luke). The pheno ypic da a comp ised
800 indi iduals om 40 amilies, which we e c ea ed in
Ap il 2013 using a pa ial ac o ial ma ing design o 35
si es and 26 dams. Each si e was ma ed o an a e age o
1.1 dams ( anging om 1 o 3) and each dam o an a e -
age o 1.5 si es ( anging om 1 o 3). The a e age num-
be o o sp ing was 22.9 pe si e ( anging om 20 o 60)
and 30.8 pe dam ( anging om 20 o 60). The pa en al
ish we e selec ed using a mul i- ai selec ion index wi h
he main weigh on imp o ed g ow h (50% o he index).
The pedig ee ile included 1661 indi iduals and nine gen-
e a ions acing back o he base popula ion es ablished in
1989 and 1990 (see Addi ional ile1).
Rea ing p o ocol
In his s udy, he p o ocols used we e app o ed by he
FGFRI Animal Ca e Commi ee, Helsinki, Finland.
The i s 6mon hs o ea ing ook place in he b eeding
nucleus, whe e he ull-sib amilies we e ea ed sepa a ely
in ound 150-L indoo anks un il agging. Va ia ion in
ea ing empe a u e ollowed a ia ion in ambien wa e -
way h oughou ha pe iod ( anging om 0 o 20°C om
he s a o ha ching un il he s a o id- agging). Du ing
he pe iod be ween Janua y 10 and 21 2014, 25 andomly
chosen ish om each s udied amily (73.6±14.4g, mean
weigh ±SD) we e indi idually agged wi h passi e in e-
g a ed ansponde s (Bioma k, Inc., Boise, Idaho, USA).
The agged ish we e anspo ed in o he communal pool
a he Laukaa ish a m, whe e hey we e ea ed unde
ambien empe a u e (1–10°C) and ligh condi ions (day
leng h 16.30–21.30h du ing he las mon h p io o he
expe imen ) un il s a o he expe imen . In June 2014,
20 agged ish pe amily we e andomly sampled o he
empe a u e ial. The ea ing empe a u es we e g adu-
ally inc eased o he expe imen al empe a u es (14 and
20°C) in he cou se o 3days. To cons uc a spli - amily
design, each o he 40 amilies was i s andomly spli
in o wo g oups o be ea ed a low and high empe a-
u es. These g oups we e e enly dis ibu ed o e 4+4
(low empe a u e) and 4+4 (high empe a u e) ound
0.4-m3 g een plas ic anks ( wo eplica e anks pe am-
ily). In o al, he empe a u e ial began wi h a o al o
800 ish, each ank con aining 50 ish ( en amilies and
i e ish om each amily).
Page 3 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
The ial was conduc ed om June 3 o Augus 12 2014.
The ish we e ed adlibi um 6h pe day (4.00 am o 10.00
am) using bel eede s wi h comme cial ou die (Rai-
sioag o L d, Finland Vi al p o LP; chemical composi ion
gi en by he manu ac u e 3.5/5.0 mm; c ude p o ein
43.0/40.0%, c ude a 28.0/30.0%, c ude ib e 1.5/1.5%, ash
6.5/6% and g oss ene gy 24.4/24MJkg−1). F om days 1 o
10, he ish we e ed wi h 3.5-mm pelle s, ollowed by a
mix u e (1:1) o 3.5- and 5.0-mm pelle s om day 11 o
20, and he ea e wi h 5.0-mm pelle s un il he end o
ial. Du ing he expe imen , daily eeding amoun was
inc eased so ha he sha e o was e eed anged om 0
o 35% o he le el o daily eed. The numbe s o unea en
pelle s we e collec ed a he ank ou le in a box wi h a
mesh bo om. The daily numbe o was e pelle s was cal-
cula ed, and hei weigh was es ima ed by mul iplying he
numbe o was e pelle s by he ai d y weigh o a pelle .
Be o e calcula ions, i e 100-pelle subsamples we e aken
om each o he die s o measu e ai d y weigh o pelle s.
The daily in ake o a ank’s popula ion was calcula ed as
he di e ence in weigh be ween he ed and was e eed.
Tanks o he low- empe a u e g oup we e supplied wi h
esh lake wa e and anks o he high- empe a u e g oups
we e supplied wi h wa e ia semi-in ensi e eci cula -
ing aquacul u e sys ems (RAS; low a e o makeup wa e
4–6m3kg−1 eed). Pu e oxygen was added o incoming
wa e o bo h empe a u e g oups o imp o e wa e oxy-
gen con en and baking soda was added o he RAS o
main ain he pH be ween 6.7 and 7.0.
Du ing he expe imen , he wa e empe a u e was
au oma ically eco ded hou ly (low- empe a u e g oup
14.1±1.0°C and high- empe a u e g oup 20.4±1.8°C;
mean±SD). Wa e oxygen sa u a ion (%) was eco ded
once e e y second week (low- empe a u e/high- em-
pe a u e; ank inle : 96.5±7.8/105.7±4.9, ank ou -
le : 78.6±6.8–83.3±7.1/82.0±3.5–86.8±5.2) and
o he wa e quali y pa ame e s we e eco ded weekly
(high empe a u e pH 6.9±0.1, o al ammonia mg L−1
(NH3+NH4) 0.05±0.04, un-ionized ammonia mg L−1
(NH3) <0.001, ni i e mg L−1 (NO2) 0.07±0.01, ni a e
mg L−1 (NO3) 4.45±0.7). A 24-h whi e ligh was p o-
ided wi h led lamps on he ank co e .
Measu emen s andcalcula ions
Indi idual ag numbe and body weigh ( o he nea es g)
we e eco ded a he beginning (129±28g; mean±SD,
n=800 ish) and end o he ial (516±98g, n=785).
Fi een ish died du ing he ial, hus only he ini ial
body weigh was a ailable o hese. Daily g ow h coe -
icien s (DGC, % day−1) o 785 ish we e calcula ed as
[17]:
DGC
=

BW1/3
2−BW1/3
1

/

×
100,
whe e BW1 and BW2 a e he body weigh o he ish a
he s a and end o he expe imen , and is he du a ion
o he expe imen (69–70days) (see Addi ional ile2).
Unlike speci ic g ow h a e (SGR), ano he widely used
measu e o ish g ow h a e, he DGC is independen o
ish body weigh and ime in e al be ween weighings
a a gi en empe a u e [17]. This was also alida ed o
ainbow ou [18].
The mean eed in ake o a ank’s popula ion pe day
(FImean, gday−1) was calcula ed as FIcum/ 1, whe e FIcum
is cumula i e eed in ake (g) o a ank’s popula ion du -
ing he pe iod o eed in ake measu emen s di ided by
he numbe o measu emen days ( 1=57d). The ela-
i e eed in ake (FI % biomass−1day−1) was calcula ed
as ollows:
100
×
FImean/[(biomass1
+
biomass2)/2]
,
whe e biomass1 and biomass2 a e he ini ial and
inal ank biomasses (g), espec i ely (see Addi ional
ile 3). Feed con e sion a io (FCR) was calcula ed as
FImean
×
/(biomass2
−
biomass1)
.
S a is ical analyses
The di e ence in DGC means be ween empe a u e
ea men s was es ed o indi idual da a using es ic ed
maximum likelihood me hod in SAS® 9.4 (MIXED p o-
cedu e; SAS® Ins i u e, Ca y, NC, USA). The model used
was:
whe e y is he obse a ion o he i h indi idual, ea -
men j is he ixed e ec o empe a u e ea men
(j=1–2), ankj is he andom e ec o ea ing ank du -
ing he ial (k=1–16), nes ed wi hin ea men , and eijk
is he andom e o e m. E o a iances we e modelled
sepa a ely o each empe a u e condi ion. In addi ion,
deg ees o eedom o he es o he ixed e ec we e
co ec ed using he me hod o Kenwa d and Roge [19].
Fo he ela i e eed in ake and FCR, ank popula ion
alues we e used as obse a ions (n=8 pe ea men
g oup) and he analysis o a iance (ANOVA) was used
o compa e he di e ences in means be ween he ea -
men g oups. No co a ia e was used in hese models.
Gene ic (co) a iance o TS ( eg ession slope) o DGC
was es ima ed using a linea andom eg ession model
(also e med as a eac ion no m model). (Co) a iance
componen s we e es ima ed by es ic ed maximum like-
lihood in ASReml 3.0 [20]. App oxima e s anda d e o s
we e calcula ed wi h ASReml acco ding o Fishe e al.
[21]. The linea andom eg ession model was as ollows:
whe e
βin
is he ixed eg ession coe icien o he
popula ion in e cep (in ) and
βsl
is he o e all ixed
eg ession slope (sl) o he ai on he h- h le els o an
(1)
yijk
=
ea men
j+
ank( ea men )k
+
eijk,
(2)
yhij
=
βin
+
βslXh
+
ai,in
+
ai,slXh
+
ehij,
Page 4 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
en i onmen al g adien Xh. Xh is he eg esso o he
en i onmen s in which he in e cep was placed ei he
on he low o high empe a u e en i onmen (a Xh=0).
The alue o Xh was 6 o high empe a u e and −6 o
low empe a u e when hese en i onmen s we e no used
a he in e cep . The scale o X is equi alen o he di -
e ence in expe imen al empe a u es, applying a uni o
1°C. The alues o 0 and 6 (o −6) we e used ins ead o
he ac ual empe a u e alues (14 and 20°C) in o de o
ha e an app op ia e in e p e a ion o he in e cep . ai
is he andom gene ic e ec o he in e cep and slope o
eac ion no m,

a, in
a, sl

∼MVN[0,A⊗G
]
, whe e MVN
is a mul i a ia e no mal dis ibu ion,
A
is he addi i e
gene ic ela ionship ma ix de i ed om he pedig ee
aced back o he base popula ion, and
G
is he addi i e
gene ic co a iance ma ix:
G
=

σ
2
a,in σa,in ,sl
σa,in ,sl σ2
a,sl 
, whe e
σ2
a,in
and
σ2
a,sl
a e he addi i e gene ic a iances o he
in e cep and slope, espec i ely, and
σa,in ,sl
is he addi-
i e gene ic co a iance be ween he in e cep and slope.
e
∼N

0,

Iσ
2
e10
0Iσ2
e2
is he andom esidual e ec
o indi idual i in en i onmen h whe e
I
is he iden i y
ma ix wi h a di e en esidual a iance o each en i-
onmen . In addi ion, he andom e m
ankk
×
ullsibl
,
accoun ing o he in e ac ion e ec o expe imen al
ank and ull-sib amily (modelled wi hou he e ec
on he slope; k=1–8 a low empe a u e and 11–18 a
high empe a u e, l=1–40), was es ed. This a iance
pa ame e ook he pe manen en i onmen e ec s in o
and ano he i e si es wi h close o ze o EBV o he slope
( he leas sensi i e) o d awing he eac ion no ms. Since
he e we e only wo en i onmen s, he EBV o DGC o
he high empe a u e en i onmen could be de i ed om
a simple equa ion:
The gene ic alues o he slope a e mul iplied by 6 o adjus
he eac ion no ms o he scale o X (change o 6°C).
Fo he in e cep o he eac ion no ms, he i abili y
(
h
2
in )
was calcula ed as:
h2
in
=

σ
2
a,in
/

σ
2
P,in
, whe e

σ2
P,in
is he
pheno ypic a iance o DGC in he in e cep en i onmen
when X=0 (equal o he sum o addi i e gene ic and esid-
ual a iance in he in e cep en i onmen :

σ2
a,in
+

σ
2
e,in
).
Because he e is no pheno ypic a iance o he slope,
he s ic sense he i abili y canno be calcula ed. The e-
o e, wo al e na i e pa ame e s we e used o desc ibe
he gene ic cha ac e is ics o TS. Following Sae-Lim e al.
[23], he he i abili y o TS (
h2
TS
) was calcula ed as:
whe e

σ2
a,sl
×

σ
2
a,X
is he addi i e gene ic a iance o he
slope mul iplied by he a iance o X, espec i ely.

σ2
X
is
equal o 18 in his s udy, since he alues o X a e 0 and
6. The s anda dized nume a o in Eq.(4) is equi alen o
he a iance o he geno ype by en i onmen (GxE) in e -
ac ion, which is independen om he di e en scales o
an en i onmen al a iable
X
. The denomina o

σ2
P,To al
was de ined as ollows:
(3)
EBV
DGC,highT =
EBV
in ,lowT +
6
×
EBV
sl
.
(4)
h
2
TS =

σ
2
a,sl ×

σ
2
a,X

σ2
P,To al
,
�
σ
2
P,To al =


(nlowT −1)
�
σ2
PDGC,lowT +
�
nhighT −1
��
σ2
PDGC,highT +nlowTnhighT
�
GlowT −GhighT
�2
/nlowT +nhighT
nlowT +nhighT −1

,
accoun , which we e caused by di e en ea ing anks
be ween and wi hin amilies. Howe e , based on he like-
lihood a io es , inclusion o he
ankk
×
ullsibl
e m
did no a ec he i o he model (χ2=0.001, p=0.486).
The e o e, he esul s a e only p esen ed o he models
in which his a iance pa ame e was omi ed.
Bo h he magni ude and sign o a gene ic co ela ion
be ween he in e cep and slope, as well as he gene ic
a iance o he ai , depend on he en i onmen o which
he in e cep is de ined [22]. The e o e, he andom eg es-
sion model was un wice, ei he wi h low
(Xh1
=
0)
o
high empe a u e ea men
(Xh2
=
0)
as he in e cep
en i onmen . The co a iance be ween es ima ed b eeding
alues (EBV) o DGC a in e cep (in ) and slope (sl) was
g aphically illus a ed by choosing i e si es wi h he high-
es absolu e EBV (i.e., gene ically he mos sensi i e si es)
whe e
n
is he numbe o indi iduals wi h a eco d o an
animal ai ,

σ2
PDGC
is he es ima ed pheno ypic a iance
o he ai and
G
is he aw pheno ypic mean o DGC.
The denomina o was de i ed om Scheine ’s app oach,
whe e he o al pheno ypic a iance ac oss en i onmen s
was calcula ed om an analysis o a iance [24]. How-
e e , i is impo an o no e ha

σ2
P,To al
is no he pheno-
ypic a iance o TS, and hus
h2
TS
is a desc ip i e a he
han a p edic i e pa ame e [24]. The de ini ion o he i -
abili y in Eq.(4) does no co espond wi h he con en-
ional de ini ion o he i abili y, which is he eg ession o
b eeding alue on pheno ype.
Following Sae-Lim e al. [23], an al e na i e measu e
ha is called co-he i abili y was de ined on he basis o
selec ion index p inciples. Co-he i abili y is exp essed
as he eg ession coe icien (b) o he b eeding alue
Page 5 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
o slope on he pheno ype P and de ines he he i able
gene ic a iance o TS o DGC when he selec ion c i e-
ion is DGC in one en i onmen . The pheno ypic a i-
ance (
σ2
P
) o a ai is:
Co-he i abili y can a y in magni ude and ha e bo h
posi i e and nega i e alues, depending on which en i-
onmen is se as in e cep en i onmen (X=0). The
sign o he co-he i abili y explains he change in co e-
la ed esponse o TS when mass selec ion o highe phe-
no ypic alues o DGC is p ac iced in one en i onmen
[25]. He e, he selec ion on DGC was assumed o be pe -
o med ei he a low o high empe a u e (in e cep en i-
onmen ; X=0), which gi es he co-he i abili y b in he
ollowing equa ion:
whe e

σ2
Ph
is he pheno ypic a iance o DGC in he selec-
ion en i onmen h. Co-he i abili y is p edic i e o
esponse o selec ion.
The gene ic co ela ion be ween in e cep and slope

G(in ,sl)
was calcula ed as:
Finally, he accu acy ( IH) o EBV o TS when DGC is
used as a selec ion c i e ion in one o he en i onmen s
is equal o:
whe e
σP
is he pheno ypic s anda d de ia ion and
σa,sl
is
he slope s anda d de ia ion. Equa ion(4) is equi alen o
ha de i ed by Kolmodin and Bijma [25].
Resul s
Means o g ow h a e, eed in ake and eed con e sion
a io
The low- empe a u e g oup had sligh ly bu signi ican ly
highe DGC means han he high- empe a u e g oup
(Table1). Fo 25 o he 40 amilies, he aw (unco ec ed)
DGC mean was highe a he lowe empe a u e (Fig.1).
In con as , bo h eed in ake (FI) and eed con e sion
a io (FCR) means we e signi ican ly lowe in he low-
empe a u e g oup (Table1).
(5)
σ2
P
=σ
2
a,in
+2Xσ
a,in ,sl
+X
2
σ
2
a,sl
+σ
2
e,
(6)
b
=
6
σ
a,in ,sl

σ2
a,in
+

σ2
e,in
=
6
σ
a,in ,sl

σ2
Ph
,
(7)
G(in ,sl)=

σain ,sl

σ2
a,in ×

σ2
a,sl
.
(8)
IH =

σa,in ,sl +X

σ
2
a,sl

σ
P

σ
a,sl
,
Gene ic (co) a iance o DGC andi s he mal sensi i i y
The he i abili y o he slope ha de ines TS was mod-
e a e (
h2
TS
= 0.24), which indica es ha he addi i e
gene ic a ia ion in TS cons i u es qui e a la ge p opo -
ion o he o al pheno ypic a ia ion in DGC ac oss
en i onmen s. The co-he i abili y o TS was mod-
e a ely nega i e (−0.28) when he lowe empe a u e
was assigned as he in e cep en i onmen . This indi-
ca es ha a mode a e accu acy o selec ion o TS o
g ow h can be achie ed when indi idual selec ion o
DGC is p ac iced in a low- empe a u e en i onmen
( IH=0.44). Ins ead, he co-he i abili y es ima e was
posi i e (0.20) when a high- empe a u e en i onmen
was used o he in e cep . This esul ed in lowe accu-
acy (0.25), compa ed o ha o selec ion a he lowe
empe a u e. Fo he DGC a he in e cep , he he i -
abili y es ima es we e simila and mode a e (
h2
in
=0.46)
a bo h empe a u es (Table 2). Thus, he he i able
Table 1 E ec o  ea ing empe a u e (lowT 14.1 °C
andhighT 20.4°C) ondaily g ow h coe icien (DGC), eed
in ake (FI) and eed con e sion a io (FCR, in ake/gain)
d =deg ees o eedom
The alues a e aw pheno ypic mean±S.D. DGC was analysed using da a om
indi idual ish, whe eas ank alues we e used as obse a ions o FI and FCR
T ea men DGC % day−1FI % biomass−1day−1FCR
LowT 4.35 ± 0.63 1.66 ± 0.05 0.88 ± 0.01
HighT 4.19 ± 0.53 1.74 ± 0.05 0.97 ± 0.02
F- a io 5.13 8.40 115.9
d 1, 13.5 1, 14 1, 14
p alue 0.041 0.012 < 0.001
Di e e
nce in DGC (highT - lowT)
Family numbe
-1.0
-0.8
-0.6
-0.4
-0.2
0.0
0.2
0.4
0.6
0.8
010203
04
0
Fig. 1 Di e ence in daily g ow h coe icien means o ainbow
ou amilies ea ed a low (14.1 °C) and high (20.4 °C) empe a-
u es. Families wi h a nega i e alue g ew be e a low han a high
empe a u e

Page 6 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
po en ial o g ow h a e did no change be ween he
wo empe a u e condi ions.
The gene ic co ela ion be ween DGC and i s TS
was signi ican and s ongly nega i e (−0.64) when he
lowe empe a u e en i onmen was used o he in e -
cep (Table2). This implies ha a high DGC a he lowe
empe a u e is gene ically associa ed wi h inc eased TS
ac oss en i onmen s. Howe e , Fig.2 shows ha he
geno ypes (si es) wi h s eep slope EBV we e no con-
sis en ly hose ha showed he as es g ow h po en ial
in he in e cep en i onmen . In ac , some geno ypes
associa ed wi h slow g ow h also showed conside able
sensi i i y o he mal change, al hough in he opposi e
di ec ion. When he in e cep was placed a he highe
empe a u e, he es ima ed gene ic co ela ion was
posi i e (0.38) al hough no s a is ically di e en om
ze o (based on he la ge s anda d e o ; Table2). Hence,
he g ow h po en ial o geno ypes a he highe em-
pe a u e may no show an associa ion wi h di e ences
in TS when he indi iduals a e mo ed o he lowe
empe a u e.
Discussion
The empe a u e di e ence o 6°C in ou expe imen
was su icien o cause subs an ial a ia ion in he g ow h
eac ion no ms among 1-yea -old ainbow ou amilies,
which indica ed he i able di e ences in hei TS. Indeed,
he TS o DGC in ol ed a conside able amoun o gene ic
a ia ion, which indica es a po en ial o esponse o a -
ge ed selec ion on TS. Bo h he desc ip i e pa ame e
h2
TS
and he co-he i abili y, which explain he he i able a i-
ance o TS o g ow h, p o ed o be mode a e. Ou ind-
ing is no consis en wi h p e ious da a in he li e a u e,
including 18 s udies on ish g ow h ai s, which showed
ha he he i abili y o mac o-en i onmen al sensi i -
i y is gene ally low [23, 24]. Fo example, Sae-Lim e al.
[23] who used a mul igene a ion da ase on Finnish ain-
bow ou did ind subs an ial addi i e gene ic a ia ion
in mac o-en i onmen al sensi i i y o body weigh , bu
he es ima ed he i abili y was low (0.07). In hei s udy,
he wo mac o-en i onmen s we e a eshwa e b eed-
ing nucleus and a sea es s a ion, which had disc e e
loca ions and di e ged in se e al en i onmen al ac o s,
including wa e salini y and empe a u e, and ea ing
sys em as a whole (ea h-bo omed aceways s. sea ne
cages, ish densi y, die and eeding in ensi y). Ou esul s
suppo he idea ha gene ic a ia ion in mac o-en i on-
men al sensi i i y would be smalle han ha in he phe-
no ypic alue o he ai a he in e cep poin [24].
Table 2 Gene ic pa ame e s and gene ic co ela ions
(± hei app oxima e s anda d e o ) be ween in e cep
andslope ob ained om he andom eg ession models
o daily g ow h coe icien (DGC) when he in e cep was
placed ei he in he low o high empe a u e en i onmen

σ2
a,in
=gene ic a iance o DGC a he in e cep poin ;

σ2
e,in
= esidual a iance
o DGC a he in e cep poin ;

σ2
a
,sl
=gene ic a iance o he eac ion no m
slope;

σ2
P,To al
= o al pheno ypic a iance o DGC ac oss en i onmen s;
h2
in
=he i abili y o DGC a he in e cep
(
σ
2
a,in
/

σ
2
P,in )
, whe e

σ2
P,in
is he
pheno ypic a iance o DGC; co-he i abili y o TS

6

σa,in ,sl

σ2
a,in +

σ2
e,in

, whe e

σa,in ,sl
is
he addi i e gene ic co a iance be ween he in e cep and slope
h2
TS
=he i abili y o he slope

σ2
a,sl×

σ2
a,X

σ2
P,To al

, whe e

σ2
a,sl
×

σ
2
a
,
X is he addi i e
gene ic a iance o he slope mul iplied by he a iance o en i onmen al alues
X
, espec i ely;
G(in ,sl)
=gene ic co ela ion be ween he in e cep and slope

σain ,sl

σ2
a,in ×

σ2
a,sl

*Es ima e ha is signi ican ly di e en om 0 (95% CI does no include ze o)
Pa ame e In e cep en i onmen
LowT HighT

σ2
a
,in
0.190 (0.063) 0.130 (0.043)

σ2
e
,in
0.221 (0.041) 0.156 (0.028)

σ2
a
,sl
0.005 (0.002) 0.005 (0.002)

σ2
P,To al
0.354 0.354
h2
in
0.463 (0.123) 0.455 (0.120)
h2
TS
0.244 0.244
Co-he i abili y o TS −0.284 (0.124) 0.197 (0.141)
G(in ,sl)
−0.643* (0.147) 0.376 (0.214)
Si e EBV o DGC
LowT High
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
Fig. 2 Gene ic eac ion no ms o en ainbow ou si es ac oss wo
empe a u e en i onmen s. Ten si es wi h he highes absolu e EBV
( i e dashed lines) and close o ze o EBV ( i e solid lines) o he slope
a e ep esen ed. The lines connec he si e EBV o daily g ow h coe -
icien (DGC) ac oss he wo empe a u e en i onmen s, when he
in e cep was placed a he lowe empe a u e (X = 0)
Page 7 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
As expec ed, in ou s udy, he ainbow ou showed, on
a e age, lowe eed in ake, as e g ow h and be e eed
con e sion a io a he lowe (14°C) han a he highe
ea ing empe a u e (20 °C). The pe cen age dec ease
in leas squa e means o DGC was 3.5 om low o high
empe a u e. Unde condi ions, wi h a no mal oxygen
con en in he wa e and a su icien amoun o ood p o-
ided, he ju enile ainbow ou a e known o pe o m
well a empe a u es o 14 o19 °C, he op imum em-
pe a u e o g ow h being a ound 17 °C; empe a u es
highe han 20°C cause as decline in g ow h a e [15, 16,
26, 27]. Fu he mo e, in gene al, eed in ake has a highe
op imum empe a u e and eed con e sion a io a lowe
op imum empe a u e han g ow h a e o ish [28]. These
ac s a e likely esponsible o he obse ed di e ences in
eed in ake, g ow h and eed con e sion a io be ween he
expe imen al empe a u es. Du ing he expe imen , he
wa e quali y pa ame e s ha we e analyzed i.e. oxygen
con en , pH and ni ogen compounds we e a a o able le -
els o salmonid aquacul u e unde bo h empe a u e con-
di ions [29–31]. Thus, i is unlikely ha o he wa e quali y
pa ame e s han empe a u e a ec ed he obse ed esul s.
Ou esul s show ha he es ima es o he gene ic
pa ame e s o DGC we e no d ama ically in luenced
by he empe a u e en i onmen s in which he ish
we e ea ed. En i onmen al s ess was epo ed o bo h
inc ease and dec ease he addi i e gene ic a ia ion
in impo an li e-his o y and mo phological ai s [32,
33]. On he one hand, he amoun o en i onmen ally-
induced a ia ion may ypically inc ease unde un a-
o able condi ions, and hus dec ease he p opo ion o
gene ic a ia ion and in u n, he es ima ed he i abili y
e.g. [34, 35]. On he o he hand, he opposi e e ec was
epo ed in some animal b eeding s udies; challenged
en i onmen s inc ease he gene ic a iance o a ai
mo e han he esidual a iance, which esul s in highe
he i abili y e.g. [36]. In his s udy, he he i abili y o DGC
(a he in e cep ) was simila o he wo empe a u es
es ed. Bo h he gene ic and esidual a iance p o ed o
be la ge a he lowe empe a u e, which was p esum-
ably a milde en i onmen in e ms o g ow h. One can
expec ha he di e ence in he i able po en ial o g ow h
(mean) mani es s i sel only a mo e ex eme empe a-
u es abo e o below he op imum.
Mul i- ai models ha e been used in many s udies on
ainbow ou o show he p esence o G×E in e ac-
ions in g ow h [37–41]. Mul i- ai and andom eg es-
sion models a e equi alen when he dimension o he
gene ic co a iance ma ix and he ixed e ec s included
in he models a e he same [7, 23]. The gene ic co ela-
ion o DGC be ween empe a u e en i onmen s was
equal o 0.47 (SE 0.20) when a bi a ia e model was used
wi h ou da a (see “Appendix”), which con i ms he
s ong e- anking o amilies ac oss he wo empe a u es
es ed. The same pa ame e es ima e can also be ob ained
om he andom eg ession model using he gene ic (co)
a iances. Consequen ly, selec ion in ei he o he em-
pe a u e en i onmen s will p esumably esul in lowe -
han-expec ed gene ic gains in he o he en i onmen , i
he G×E in e ac ion is no aken in o accoun [41–43].
Al hough he gene ic co ela ion ha is es ima ed om a
mul i- ai model does exp ess he deg ee o e- anking
among amilies, i does no desc ibe how mac o-en i on-
men al sensi i i y o he ai can ac ually e ol e ac oss
en i onmen s. One ad an age o he andom eg ession
model is ha he gene ic pa ame e s o mac o-en i on-
men al sensi i i y o a gi en ai can be ob ained di ec ly,
which allows implemen a ion o mac o-en i onmen al
sensi i i y as a ai in he selec ion index [5, 12, 23]. Ye ,
an assump ion o his in ou s udy is ha he slopes, es i-
ma ed om he wo en i onmen poin s, a e linea .
En i onmen al sensi i i y was gene ally shown o
inc ease in esponse o selec ion o high pheno ypic
alues when G × E in e ac ion is p esen [5, 6, 44].
Acco ding o Jinks and Connolly [45], his should be ue
especially when selec ion o a high pheno ypic alue
occu s in an en i onmen ha p oduces a pheno ype
wi h a highe alue compa ed o ano he en i onmen
(syne gis ic selec ion). Co espondingly, selec ion o
dec eased en i onmen al sensi i i y may gene ally esul
in educed mean p oduc i i y in mo e a o able en i on-
men s [46]. In his s udy, he gene ic co ela ion be ween
DGC (a he in e cep ) and i s TS (slope) was ma kedly
nega i e, when he in e cep was placed a he lowe em-
pe a u e. This inding is consis en wi h he assump ion
o Jinks and Connolly [45]: selec ion o as g ow h in a
mo e a o able empe a u e en i onmen should a o
inc eased sensi i i y, ha is, geno ypes ha ing s eep
nega i e slopes in eac ion no ms. Howe e , gene ically,
he mos sensi i e geno ypes wi h he s eepes slope EBV
may no consis en ly ha e highe gene ic po en ial o
g ow h a he lowe empe a u e, compa ed o he leas
sensi i e geno ypes wi h la slope EBV (Fig.2). In ac ,
some o he geno ypes wi h a slow g ow h a he lowe
empe a u e also seem o exhibi p onounced sensi i -
i y o he mal change, bu in he posi i e di ec ion (i.e.,
g owing as e a he highe empe a u e). Nega i e
gene ic ela ionships be ween p oduc ion ai s and TS
ha e also been epo ed in e es ial a m animals. Fo
example, in pigs, a gene ic co ela ion o −0.5 be ween
ca cass weigh and sensi i i y o hea s ess was epo ed
[47]. In dai y ca le, gene ic co ela ions be ween milk
yield and hea ole ance anged om −0.30 o −0.45 [48,
49], whe eas, in sheep, his gene ic co ela ion was equal
o −0.8 [50]. The obse ed nega i e gene ic co ela ion
be ween DGC and i s TS and he p esence o s ong
Page 8 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
G×E in e ac ion sugges ha selec ion decisions should
be based on mo e han one he mal en i onmen only.
Howe e , by applying a es ic ed selec ion c i e ion,
he app op ia e index weigh s ha p oduce he desi ed
gene ic esponses in bo h g ow h a e and i s TS can be
ob ained [51]. I would hen be possible o simul ane-
ously imp o e he g ow h a e ac oss en i onmen s and
cons ain he gene ic change in TS.
In addi ion o he nega i e gene ic co ela ion be ween
DGC and i s TS, he es ima ed co-he i abili y o TS was
also nega i e when a lowe empe a u e was used as he
in e cep en i onmen . Co-he i abili y is an app oxima e
measu e o he inhe i ance o he associa ion be ween
DGC and i s TS, when he selec ion c i e ion is DGC in
one empe a u e en i onmen . The co-he i abili y has he
same sign as he co ela ed esponse o di ec selec ion,
and, unlike
h2
TS
and gene ic co ela ion, his pa ame e also
e lec s he accu acy o selec ion [52, 53]. Ou esul s a e
in line wi h a ecen su ey on aquacul u e s udies by Sae-
Lim e al. [23], which showed ha he g ow h o ainbow
ou in one en i onmen is gene ically ela ed o mac o-
en i onmen al sensi i i y ac oss en i onmen s. Howe e ,
he co ela ed esponse o TS is less p onounced i selec-
ion o imp o ed g ow h a e occu s a he highe em-
pe a u e. In his case, he es ima ed co-he i abili y was
also associa ed wi h ela i ely la ge s anda d e o s, which
sugges s ha i should be ea ed wi h cau ion. The magni-
ude o he co-he i abili y gene ally inc eases, i espec i e
o i s sign, wi h an inc ease in G×E in e ac ion [23].
In his s udy, mac o-en i onmen al sensi i i y o each
geno ype ( ish amily) was de ined as he di e ence in
DGC be ween wo empe a u es. The eac ion no m
slope is no an indi idual measu e, bu i s b eeding alue
can only be es ima ed based on he g ow h eco ds o el-
a i es in wo (mac o-)en i onmen s. Because he mac o-
en i onmen al sensi i i y is basically a p ogeny ai , he
accu acy o selec ion is ac ually highe o he pa en s
han o hei o sp ing (which a e used as b eeding can-
dida es). Rainbow ou , as many o he aquacul u e spe-
cies, p oduces la ge amilies, which e ec i ely con ibu e
o he gene ic analysis o mac o-en i onmen al sensi i -
i y. Since he co-he i abili y o TS p o ed o be mode a e,
ansla ing his in o mode a e accu acy o selec ion, e y
la ge amily sizes a e no equi ed o each mode a e- o-
high p ecision in slope EBV.
Fo a ainbow ou b eede , a s ock pe o ming well
ac oss mul iple empe a u es is he mos desi able ou -
come. The leas sensi i e amilies wi h la slopes o
eac ion no ms could be selec ed when he b eeding goal
is o ob ain obus ish ha h i e unde a iable empe a-
u e condi ions (inc eased s abili y). Al e na i ely, amilies
wi h posi i e g ow h esponses a highe (o lowe ) em-
pe a u es can be chosen when de eloping a locally-adap ed
popula ion o a ce ain en i onmen . In he la e case, TS
can be iewed a he as an ad an ageous cha ac e o be
used by selec i e b eeding when imp o ing he ‘ i ’ be ween
he selec ed ish and he he mal en i onmen in which
hey a e ea ed [54]. Ei he way, i is likely ha he e will be
a high demand o mo e hea - ole an popula ions o ain-
bow ou in he u u e since empe a u es will con inue o
inc ease a ound he wo ld due o global wa ming.
This s udy was unde aken as pa o a capaci y build-
ing p ojec wi h he Resea ch Ins i u e o Aquacul u e No.
1 (RIA-1) in No he n Vie nam whe e a na ional b eeding
p og am o ainbow ou was ecen ly es ablished om he
Finnish b oods ock (Resea ch Cen e o Cold Wa e Aqua-
cul u e Species, RIA-1). Vie nam is es ima ed o be one o
he wo ld’s mos ulne able a eas o he nega i e impac s
due o clima e change. This is he case, in pa icula , wi h
cold wa e aquacul u e, o which empe a u e and wa e
a ailabili y a e he main limi ing ac o s [55]. The ish used in
his expe imen sha ed ela edness wi h he RIA-1’s b ood-
s ock. Combining ou esul s wi h he eco ds o ish pe -
o mance in Vie nam unde highe empe a u es will enable
he assessmen o selec i e b eeding possibili ies in o de o
dec ease TS in he nex b eeding gene a ions. This will aid in
expanding ainbow ou p oduc ion o lowe la i udes and
al i udes wi h be e and mo e s able wa e esou ces, and
he ish a ming sec o o adap o clima e change.
Conclusions
We ound ha he 1-yea -old ainbow ou exhibi sub-
s an ial gene ic a ia ion in g ow h esponses ac oss
di e en ea ing empe a u es. In e ms o g ow h and
eed con e sion e iciency, he ish pe o med be e
p edominan ly unde he lowe (14°C) han he highe
empe a u e condi ions (20°C). Owing o la ge addi i e
gene ic a ia ion, pe manen changes in TS o g ow h a e
possible in he s udied popula ion. The e is a ade-o
be ween g ow h a e and i s TS, since s ong selec ion o
as e g ow h a he lowe and mo e a o able empe a-
u e will p esumably esul in less empe a u e- ole an
ish. Howe e , he co ela ed gene ic change in TS could
be e ec i ely con olled while selec ing o high g ow h
ac oss en i onmen s, especially i slope EBV a e inco po-
a ed in o he selec ion index wi h app op ia e weigh ing.
Page 9 o 11
Janhunen e al. Gene Sel E ol (2016) 48:94
Au ho s’ con ibu ions
All au ho s pa icipa ed in planning he s udy. MJ, HV, NHN, HK and AN con-
ibu ed o da a collec ion. MJ and JK pe o med da a analysis. MJ was mainly
esponsible o d a ing he manusc ip , and JK, HV, NHN, AN and NPT ook
pa in w i ing and commen ing he ex . All au ho s ead and app o ed he
inal manusc ip .
Au ho de ails
1 Biome ical Gene ics, Na u al Resou ces Ins i u e Finland (Luke), Mylly ie 1,
31600 Jokioinen, Finland. 2 Aquacul u e, Na u al Resou ces Ins i u e Finland
(Luke), Su on ie 9 A, 40500 Jy äskylä, Finland. 3 Resea ch Ins i u e o Aqua-
cul u e No. 3 (RIA-3), Nha T ang, Khanh Hoa, Vie nam. 4 Te o Fish Fa m, Na u al
Resou ces Ins i u e Finland (Luke), Huuh ajan ie 160, 72210 Te o, Finland.
5 Resea ch Ins i u e o Aquacul u e No. 1 (RIA-1), Dinh Bang, Tu Son, Bac Ninh,
Vie nam.
Acknowledgemen s
This expe imen was ca ied ou as a pa o he ICI p ojec “Capaci y building
o he de elopmen o selec i e b eeding p og am in Vie nam, special ocus
on global change and en i onmen al sus ainabili y”. The s a s a he Te o
and Laukaa ish a ms p o ided he expe ise o main ain he expe imen .
MJ would like o hank Panya Sae-Lim o his ad ice on he gene ic analysis
in ASReml and Timo Pi känen o his ad ice conce ning he s a is ics. Fou
anonymous e e ees ga e aluable commen s on he p e ious d a s o he
manusc ip . The inancial suppo o he s udy was p o ided by he Minis y
o Fo eign A ai s o Finland.
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
A ailabili y o da a and ma e ials
The da ase (s) suppo ing he conclusions o his a icle is(a e) included wi hin
he a icle (and i s addi ional ile(s)).
Appendix
In a mul i- ai model, a ai ha is eco ded in di e -
en en i onmen s is ea ed as sepa a e ai s (see Addi-
ional ile4). Then, he magni ude o he e- anking o
he gene ic g oups can be quan i ied by calcula ing he
gene ic co ela ion ( G) o he ai in each pai o he
en i onmen s [42, 56]. A mul i- ai animal mixed model
was used in his s udy and un using ASReml 3.0. The
bi a ia e model was as ollows:
whe e yij is he obse a ion o he i h indi idual o he
k h ai (DGC being eco ded in wo he mal en i on-
men s), μ is an o e all ai mean, aiis he andom addi-
i e gene ic e ec o he i h indi idual, and eij is he
andom esidual e ec . I was assumed ha he andom
a iable a is mul i-no mally dis ibu ed wi h a mean o 0
yij =µ+ai+eij,
and a iance
A⊗G
, whe e
A
is he addi i e gene ic ela-
ionship ma ix de i ed om he pedig ee aced back o
he base popula ion and
G
is he addi i e gene ic (co) a i-
ances ma ix. In his s udy:
whe e
σ2
a,lowT
and
σ2
a,highT
a e he addi i e gene ic a i-
ances o DGC measu ed a low and high empe a u es,
espec i ely, and
σa,lowT,a,highT
is he addi i e gene ic
co a iance be ween low and high empe a u es. The
esidual (co) a iance ma ix is:
whe e
σ2
e,lowT
and
σ2
e,highT
a e he esidual a iances a low
and high empe a u es, espec i ely. Because each indi-
idual ish was p esen only in one empe a u e en i on-
men , he esidual co a iance be ween empe a u es was
se o 0.
Fo bo h DGC ai s, he he i abili y was calcula ed as:
whe e
σ2
P
is he pheno ypic a iance (sum o addi i e
gene ic and esidual a iances), i.e.
σ2
a
+σ
2
e
.
The gene ic co ela ion (
G
) be ween DGC measu ed
in wo empe a u e en i onmen s was calcula ed as:
whe e
σa,lowT,a,highT
is he co a iance be ween addi i e
gene ic alues measu ed a low and high expe imen-
al empe a u es, and
σ2
a,lowT
and
σ2
a,highT
a e he addi-
i e gene ic a iances o DGC measu ed a low and
high empe a u es, espec i ely. The gene ic pa ame e s
es ima ed using a bi a ia e animal model a e shown in
Table3.
G
=

σ2
a,lowT σa,lowT,a,highT
σa,lowT,a,highT σ2
a,highT
,
R
=

σ2
e,lowT 0
0σ2
e,highT
,
h2
=σ
2
a
/σ
2
P,
G=
σ
a,lowT,a,highT

σ2
a,lowT ×σ2
a,highT
,
Table 3 Gene ic pa ame e es ima es (± hei app oxi-
ma e s anda d e o s) o  DGC in wo he mal en i on-
men s using a bi a ia e animal model
Pa ame e DGC lowT DGC highT
σ2
a
0.130 (0.043) 0.190 (0.063)
σ2
e
0.156 (0.028) 0.221 (0.041)
σ2
P
0.286 (0.026) 0.411 (0.038)
h20.455 (0.120) 0.463 (0.123)
G
0.468 (0.197)
Addi ional iles
Addi ional ile1. Pedig ee o he s udied ainbow ou .
Addi ional ile2. Indi idual measu emen da a o uni a ia e gene ic
analyses.
Addi ional ile3. Tank mean alues o FI and FCR.
Addi ional ile4. Indi idual measu emen da a o mul i a ia e gene ic
analysis.