Estimates of recent and historical effective population size in turbot, seabream, seabass and carp selective breeding programmes

Sau ae al. Gene Sel E ol (2021) 53:85
h ps://doi.o g/10.1186/s12711-021-00680-9
SHORT COMMUNICATION
Es ima es o  ecen andhis o ical e ec i e
popula ion size in u bo , seab eam, seabass
andca p selec i e b eeding p og ammes
Ma ía Sau a1* , A mando Caballe o2, En ique San iago3, Almudena Fe nández1, Elisabe h Mo ales‑González1,
Jesús Fe nández1, San iago Cabalei o4, Ad ián Millán5, Paulino Ma ínez6, Ch is os Palaiokos as7,
Ma in Kocou 8, Muhammad L. Aslam9, Ross D. Hous on7, Ma in P chal8, Luca Ba gelloni10, Kos as Tzokas11,
Pie ick Ha ay12, Jean‑Sebas ien B uan 13 and Bea iz Villanue a1
Abs ac
Backg ound: The high ecundi y o ish species allows in ense selec ion o be p ac ised and he e o e leads o
as gene ic gains. Based on his, nume ous selec i e b eeding p og ammes ha e been s a ed in Eu ope in he las
decades, bu in gene al, li le is known abou how he base popula ions o b eede s ha e been buil . Such knowledge
is impo an because base popula ions can be c ea ed om e y ew indi iduals, which can lead o small e ec i e
popula ion sizes and associa ed educ ions in gene ic a iabili y. In his s udy, we used genomic in o ma ion ha was
ecen ly made a ailable o u bo (Scoph halmus maximus), gil head seab eam (Spa us au a a), Eu opean seabass
(Dicen a chus lab ax) and common ca p (Cyp inus ca pio) o ob ain accu a e es ima es o he e ec i e size o com‑
me cial popula ions.
Me hods: Res ic ion‑si e associa ed DNA sequencing da a we e used o es ima e cu en and his o ical e ec i e
popula ion sizes. We used a no el me hod ha conside s he linkage disequilib ium spec um o he whole ange
o gene ic dis ances be ween all pai s o single nucleo ide polymo phisms (SNPs), and hus accoun s o po en ial
luc ua ions in popula ion size o e ime.
Resul s: Ou esul s show ha he cu en e ec i e popula ion size o hese popula ions is small (equal o o less
han 50 ish), po en ially pu ing he sus ainabili y o he b eeding p og ammes a isk. We ha e also de ec ed impo ‑
an d ops in e ec i e popula ion size abou i e o nine gene a ions ago, mos likely as a esul o domes ica ion and
he s a o selec i e b eeding p og ammes o hese species in Eu ope.
Conclusions: Ou indings highligh he need o b oaden he gene ic composi ion o he base popula ions om
which selec ion p og ammes s a , and sugges ha measu es designed o inc ease e ec i e popula ion size wi hin
all a med popula ions analysed he e should be implemen ed in o de o manage gene ic a iabili y and ensu e he
sus ainabili y o he b eeding p og ammes.
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Backg ound
The success o any b eeding p og amme depends c i i-
cally on how he base popula ion o b eede s is buil ,
since he gene ic a iabili y ha is ini ially a ailable in
he ounde s will a ec he gene ic p og ess achie ed
in he subsequen selec ion p og amme [1–3]. This is
Open Access
G
ene ics
S
elec ion
E olu ion
*Co espondence: [email p o ec ed]
1 Depa amen o de Mejo a Gené ica Animal, INIA‑CSIC, C a. de La
Co uña, km 7.5, 28040 Mad id, Spain
Full lis o au ho in o ma ion is a ailable a he end o he a icle
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Sau ae al. Gene Sel E ol (2021) 53:85
pa icula ly impo an in aquacul u e because, gi en
he high ecundi y o ish species, base popula ions can
be c ea ed om e y ew indi iduals, which would lead
o small e ec i e popula ion sizes (Ne) and he e o e,
o high a es o loss o gene ic a iabili y, high a es o
inb eeding and es ic ed long- e m selec ion esponses.
Wi h he apid de elopmen o genomic ools, empo-
al se ies o Ne can be es ima ed o gene a ions be o e
pedig ee eco ding began. This is o g ea impo ance in
aquacul u e species o de e mine he impac o domes i-
ca ion on he gene ic a iabili y p esen in he base popu-
la ions and he po en ial long- e m esponse o selec ion.
Genomic es ima es o Ne a e ob ained based on he
linkage disequilib ium (LD) app oach [4], and di e en
me hods ha e been de eloped o es ima e his pa ame e
ac oss gene a ions. These me hods ha e assumed ha
he Ne o a pa icula gene a ion in he pas can be es i-
ma ed om LD be ween pai s o single nucleo ide poly-
mo phisms (SNPs) sepa a ed by a speci ic dis ance [5].
Howe e , his assump ion implies ha he demog aphic
e en s ha occu ed in ha pa icula gene a ion do no
a ec subsequen gene a ions, and he me hod only holds
o linea changes in popula ion size [5]. To ci cum en
his p oblem, San iago e al. [6] ha e ecen ly de eloped
an app oach whe e he LD spec um o he whole ange
o ecombina ion a es be ween all pai s o SNPs is aken
in o accoun o es ima ing Ne in consecu i e gene a-
ions, and his allows he de ec ion o d as ic changes in
popula ion size.
In spi e o he impo ance o es ima ing Ne, es ima es
o his pa ame e a e sca ce o mos aquacul u e spe-
cies. In his s udy, we used genomic in o ma ion ha was
ecen ly p oduced o impo an ish species in Eu o-
pean aquacul u e ( u bo , gil head seab eam, Eu opean
seabass and common ca p) o ob ain ecen and his o i-
cal es ima es o Ne o comme cial popula ions, using
he no el me hod de eloped by San iago e al. [6]. These
es ima es a e use ul o e alua e he cu en gene ic s a-
us o he popula ions and o iden i y pas changes in Ne
po en ially associa ed wi h domes ica ion o wi h he
es ablishmen o selec i e b eeding p og ammes.
Me hods
Da a
Da a we e de i ed om b oods ock (and hei o sp ing)
sampled in 2014 om di e en Eu opean b eeding p o-
g ammes o u bo , gil head seab eam, Eu opean sea-
bass and common ca p wi hin he amewo k o he
FISHBOOST p ojec (www. ishb oos . eu) (Table1). Un e-
la ed b oods ock we e ma ed and hei o sp ing we e
used o di e en expe imen al pu poses. Genomic in o -
ma ion was a ailable o bo h pa en s and hei o sp ing.
Geno ypes we e ob ained using educed ep esen a ion
geno yping app oaches [speci ically RAD sequencing,
(RAD-seq)]. The species’ linkage maps and e e ence
genomes we e used o map he SNPs [7–10]. De ails on
he numbe o samples and SNPs a ailable o each popu-
la ion analysed a e summa ised in Table1. Geno yping
and il e ing de ails a e desc ibed elsewhe e o u bo
[7], seab eam [8], seabass [9] and ca p [10]. Impu a ion o
missing geno ypes, which was only pe o med o u bo ,
was ca ied ou using he so wa e BEAGLE 4.1 [11].
Tu bo samples we e ob ained om an expe imen-
al popula ion o A lan ic o igin main ained a CETGA
(Aquacul u e Clus e o Galicia, Spain) h ough hie a -
chical ma ings. Fo gil head seab eam, da a came om
one o he ou gene ically linked yea ly coho s o he
b eeding nuclei o he And omeda G oup SL (G eece)
and Fe me Ma ine de Douhe (FMD, F ance), whe e he
main b eeding objec i es in he selec ion p og ammes
a e g ow h and body shape. The And omeda p og amme
applies mass spawning, while he FMD p og amme
applies pa ial ac o ial ma ing designs [8]. Eu opean
seabass samples came also om one o he ou linked
yea ly coho s o he FMD b eeding nucleus, whe e he
b eeding objec i es a e g ow h and body shape. In his
p og amme, pa ial ac o ial ma ings a e also applied [9].
Finally, o common ca p, samples we e ob ained om
he Amu Mi o ca p (Vodňany line), which was ecen ly
Table 1 Desc ip ion o samples and genomic in o ma ion o he popula ions analysed
Numbe o o sp ing (No ) and pa en s (Npa , including si es and dams) wi h geno ypes a ailable, numbe o SNPs (nsnp) and linkage g oups (nlg), gene ic (cM) and
physical (Mb) genome size and esul ing SNP densi y (d, in SNPs pe Mb) o each popula ion
a Es ima es aken om he li e a u e ([44] o u bo ; [45] o seab eam; [46] o seabass; [47] o ca p)
Popula ion No Npa (♂, ♀)nsnp nlg cM Mb d
Tu bo 1391 46 (23, 23) 18,097 22 1403 568 32
Seab eam_A 724 117 (57, 59) 15,184 24 1406 790a19
Seab eam_F 881 107 (71, 22) 21,701 24 1970 790a28
Seabass 1308 65 (48, 17) 8014 24 1373a577 14
Ca p 1349 60 (40, 20) 12,311 50 3944 1830a7
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Sau ae al. Gene Sel E ol (2021) 53:85
c ea ed a he Uni e si y o Sou h Bohemia in České
Budějo ice. Fo his line, F1 o sp ing we e ob ained om
c osses be ween emales om a cul u ed popula ion
(o igina ing om Hunga y and Ge many) wi h a mi o
pheno ype o scaliness and males om a wild popula ion
( om he Amu i e , Sibe ia) wi h a scaly pheno ype.
The Amu Mi o s ain was ounded om F2 c osses by
selec ing o sp ing ha had he mi o pheno ype. The
popula ion used in his s udy was ob ained by a i icial
e iliza ion ha in ol ed ou blocks o ull ac o ial
c osses each comp ising i e dams and en si es [10].
Es ima ion o linkage disequilib ium ande ec i e
popula ion size
Es ima es o LD be ween pai s o loci and empo al es i-
ma es o Ne we e ob ained using he so wa e GONE and
i s auxilia y p og ams de eloped by San iago e al. [6]
(a ailable in h ps:// gi hub. com/ es ud/ GONE). Squa ed
co ela ions be ween allele equencies o pai s o SNPs
( 2; [12]) we e ob ained o all pai s o SNPs wi hin each
linkage g oup (ch omosome). Ca ego y bins o di e en
anges o gene ic dis ances (in Mo gans) be ween SNPs
we e buil and he a e age alues o d2 ( he a e age o 2
alues be ween pai s o SNPs weigh ed by hei a iance
in allele equences; [13]) we e ob ained o each bin. The
me hod in ol es a gene ic algo i hm o in e he his o i-
cal se ies o Ne in he popula ion ha minimises he sum
o he squa ed di e ences be ween he obse ed alues o
d2 o he bins and hose p edic ed conside ing di e en
demog aphic his o ies. The analyses assumed ha phase
is unknown and he gene ic dis ances be ween SNPs
we e co ec ed by Haldane’s unc ion. Fo he emaining
so wa e op ions, he de aul alues we e used. In o de
o compa e ou esul s wi h hose o o he s udies, pa -
e ns o LD measu ed as 2 ac oss physical dis ance we e
ep esen ed o he popula ions o which he physical
posi ion o SNPs was a ailable on he e e ence genome
assemblies (i.e. u bo GCA_003186165.1 and seabass
GCA_000689215).
Fo he sake o compa ison, empo al es ima es o
ances al Ne we e also ob ained using he p e ious
me hod o Hayes e  al. [5] as implemen ed by Sau a
e al. [14]. Al hough bo h he GONE me hod and ha
o Hayes e al. [5] a e based on he well known ela ion-
ship be ween LD and Ne [4], he main di e ence be ween
hem is ha he o me assumes cons an Ne o linea
changes in Ne.
Resul s
The pa e n o LD decay wi h physical dis ance ha
was compu ed wi h o sp ing da a o u bo and sea-
bass is ep esen ed in Fig.1. O e all, he a e age LD ( 2)
be ween SNPs sepa a ed by sho dis ances (< 0.01kb)
was mode a ely low (0.15 o u bo and 0.24 o seabass)
and dec eased apidly wi h physical dis ance. The a e age
2 was educed by hal in bo h cases o dis ances sho e
han 5kb.
Es ima es o ecen Ne we e equal o o less han 50
ish in all cases. When using o sp ing da a, Ne o 31 o
u bo , 46 o seab eam_A, 32 o seab eam_F, 40 o sea-
bass and 33 o ca p we e ound, and when using pa en s
da a, he co esponding alues we e 26, 50, 30, 32 and 15,
espec i ely.
Es ima es o his o ical Ne we e la ge han 1000 ish o
abou 20 gene a ions ago in all species. Howe e , impo -
an d ops we e obse ed abou i e gene a ions ago o
u bo and seab eam and abou eigh o nine gene a ions
ago o seabass, using da a om pa en s o om o sp ing
(Fig.2 and see Addi ional ile1: Fig. S1). The wo popula-
ions o seab eam showed a simila pa e n o Ne decay.
Es ima es o ances al Ne a e no p o ided o ca p since
he Amu Mi o s ain comes o iginally om c osses o
se e al s ains, and unde a scena io o s ong and ecen
popula ion admix u e, he me hod o es ima e his o ical
Ne is no concep ually applicable. Howe e , es ima es o
con empo a y Ne can be ob ained in his case, al hough
he es ima es a e likely o be biased downwa ds because
o popula ion admix u e [15].
The LD me hod o Hayes e al. [5] led o linea ends in
his o ical Ne, as expec ed (see Addi ional ile2: Fig. S2),
which con as s wi h he d as ic d ops shown in Fig.2.
His o ical alues es ima ed wi h his me hod o he
ea lies gene a ion shown (gene a ion 100) we e smalle
han 1000 indi iduals, i.e. much smalle han hose
ob ained by GONE in Fig.2. Howe e , ecen Ne alues
wi h he same me hod (44 o u bo , 33 o seabass, 51
o seab eam_A, and 49 o seabass_F) we e o he same
o de o magni ude as hose ob ained wi h he me hod o
San iago e al. [6] and a e shown in Fig.2.
Discussion
In his s udy, ecen and his o ical Ne es ima es we e
ob ained o a med popula ions o impo an Eu opean
aquacul u e species ( u bo , gil head seab eam, Eu opean
seabass and common ca p), using genome-wide SNP da a
om RAD-seq, and a no el accu a e me hod based on
LD measu es [6]. Ou esul s e ealed ha ecen Ne o
all he analysed popula ions we e small and ha impo -
an d ops in ances al Ne occu ed in hese popula ions
abou i e o nine gene a ions ago.
Recen Ne es ima es o all he analysed popula ions
we e equal o o less han 50 ish. A alue a ound 50 is
conside ed o i he minimum alue ecommended o
a oid se e e inb eeding dep ession and e ain i ness in
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Sau ae al. Gene Sel E ol (2021) 53:85
he sho - e m [16–18]. Howe e , ou Ne es ima es o
seab eam and seabass could be sligh ly unde es ima ed
gi en ha he da a used came om b eeding schemes
wi h o e lapping gene a ions and he me hod asumes
disc e e gene a ions [6, 19].
In gene al, he magni ude o ou ecen es ima es o Ne
was wi hin he ange o hose ound in o he a med ish
popula ions o di e en species [20–30], al hough he e
a e excep ions [31]. Fo ins ance, he es ima e o Ne in he
GIFT (Gene ically Imp o ed Fa med Tilapia) selec ion
p og amme in which he c ea ion o he base popula ion
was ca e ully planned, was equal o 88 a e se en gen-
e a ions o selec ion o g ow h a e [31]. The small es i-
ma es o Ne ob ained o he a med popula ions analysed
he e con as wi h he la ge es ima es (> 1000) ound o
wild popula ions o u bo , seabass and seab eam [32–
34]). Al hough es ima es o Ne o he wild common ca p
a e no a ailable, gene ic a iabili y analyses ha e shown
ha hey a e smalle in a med han in wild s ains [35,
36].
Es ima es o his o ical Ne o all he analysed popula-
ions e ealed impo an d ops occu ing abou i e o
nine gene a ions ago. We ob ained simila esul s using
da a om he educed numbe o pa en al samples o
om he mo e ex ensi e numbe o o sp ing samples
(Fig.2). The powe o he me hod o de ec luc ua ions
in Ne is p opo ional o he p oduc o he sample size
and he squa e oo o he numbe o ma ke s di ided by
Fig. 1 Decay o a e age linkage disequilib ium ac oss ch omosomes measu ed as 2 agains physical dis ance. Physical dis ance in e ms o
agmen leng h is indica ed in Mb o he species o which a physical map is a ailable; i.e. u bo (le panels) and seabass ( igh panels). Th ee
di e en dis ance ca ego ies a e ep esen ed: a om 0.0 o 0.5 Mb; b om 0.5 o 5 Mb; c om 5 o 20 Mb
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Sau ae al. Gene Sel E ol (2021) 53:85
Ne, and he minimum alue o ensu e accu a e es ima-
ions o Ne is 100 [6]. Using pa en al samples, he alue
was much la ge han 100, and hus es ima es ob ained
om pa en s we e as eliable as hose ob ained om
o sp ing.
A d op in Ne and he consequen d op in gene ic a i-
abili y in a med popula ions can occu du ing he es ab-
lishmen o he base popula ion ( ounde e ec ) bu also
in subsequen gene a ions o selec ion i he e is no op i-
mal inb eeding con ol. Some cau ion mus be aken in
he in e p e a ion o he d ops obse ed as hey could
also be a consequence o popula ion admix u e o o he
use o inaccu a e gene ic maps [6]. Ne e heless, ou
esul s a e highly consis en wi h he in o ma ion abou
he o igin o b oods ock and how hese p og ammes
ha e been un. Al hough limi ed, he a ailable in o -
ma ion sugges s ha he domes ica ion o u bo , gil -
head seab eam and Eu opean seabass s a ed a ound
he 1970s, and ha selec i e b eeding p og ammes o
inc easing g ow h a e s a ed in he 1990s [37], wi h
app oxima ely ou o six gene a ions o selec ion o da e
o he popula ions analysed he e. Unde his b oad con-
ex , ou es ima es o his o ical Ne sugges ha he com-
bina ion o bo h domes ica ion and he s a o selec ion
p og ammes is he mos likely explana ion o he impo -
an ecen d ops in e ed in he popula ions analysed.
Bo h e en s may ha e occu ed oo close in ime o be
disen angled by he me hod.
Ou esul s e lec a mode a ely low LD be ween SNPs
ha a e sepa a ed by e y sho dis ances in u bo and
seabass popula ions. In addi ion, a e y as LD decay
wi h physical dis ance was obse ed in bo h popula-
ions. In ac , 2 dec eased by hal a dis ances sho e
han 0.02Mb and i was main ained when he dis ance
inc eased by one o de o magni ude. A dis ances longe
han 10Mb, 2 eached alues lowe han 0.05. Simila
LD alues ha e been epo ed o coho salmon [29] and
Nile ilapia [38] a sho dis ances bu he a e o dec ease
in LD was much slowe han hose obse ed he e o u -
bo and seabass. Much highe alues o LD (> wo old o
sho dis ances) ha e been epo ed in a med popula-
ions o A lan ic salmon [28, 39, 40] and ainbow ou
[30], wi h also LD emaining highe o e much longe
dis ances. These esul s may sugges ha highe LD al-
ues a e obse ed in popula ions wi h a longe his o y o
a i icial selec ion.
As al eady men ioned, an impo an limi a ion o
he LD me hod o Hayes e al. [5] o es ima e his o ical
Ne is ha i only holds o linea changes in popula ion
size. Indeed, p e ious s udies applying his me hod ha e
obse ed linea ends in Ne o e ime [28–31], as we
obse ed when eanalysing ou da a applying his me hod
(see Addi ional ile2: Fig. S2). As e lec ed in ou esul s,
he me hod by San iago e al. [6] p o ides in his case, a
mo e p ecise iew o he d as ic changes in he his o ical
Ne, such as hose obse ed in Fig.2. Ano he di e ence
Fig. 2 Es ima es o Ne (loga i hmic scale) ac oss he las 20 gene a ions o each popula ion analysed. S aigh lines ep esen es ima es ob ained
using da a om pa en s and dashed lines ep esen es ima es ob ained using da a om o sp ing

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Sau ae al. Gene Sel E ol (2021) 53:85
be ween he esul s o he wo me hods conce ns he
la ge disc epancy be ween he his o ical es ima es o Ne
(see Addi ional ile1: Fig. S1 and Addi ional ile2: Fig.
S2). In o de o shed some ligh on his issue, we ca ied
ou compu e simula ions unde a scena io ha mim-
ics he pa e n obse ed in Fig.2 (see Addi ional ile3:
Fig. S3 o esul s and simula ion de ails). In he simula-
ions, a la ge popula ion wi h a cons an size N o 1000
o 10,000 suddenly d ops o N = 100 o 50 indi iduals in
he las en o i e gene a ions, espec i ely. We epea ed
his simula ion 20 imes and ca ied ou analyses wi h he
me hods o San iago e al. [6] (using GONE) and Hayes
e al. [5]. The simula ions show ha he me hod o Hayes
e al. [5] does no e lec he sudden d op in popula ion
size, and ha i gi es e y downwa dly biased es ima es
o he his o ical size. The simula ions also show ha he
ances al Ne ob ained by GONE can be o e es ima ed,
pa icula ly when he size o he ances al popula ion
is la ge. Thus, he la ge obse ed alues o ances al Ne
shown in Fig.2 and Addi ional ile2: Fig S2 should be
aken wi h cau ion, since hey can be o e es ima ions. In
any case, GONE is able o de ec he d as ic change in Ne
as e lec ed in bo h igu es.
Conclusions
In summa y, ou esul s sugges ha he cu en Ne o
he comme cial popula ions analysed he e a e, in gene al,
below he c i ical alue o 50 indi iduals ha is ecom-
mended o ensu e sho - e m sus ainabili y o selec ion
p og ammes. Se ies o his o ical Ne e eal impo an
d ops p obably due o domes ica ion and he s a o
b eeding p og ammes. Ou indings highligh he need
o b oadening he gene ic composi ion o base popula-
ions om which selec ion p og ammes s a and sug-
ges ha measu es o inc ease Ne wi hin all he a med
popula ions analysed he e should be implemen ed. These
measu es include inc easing he numbe o pa en s
selec ed, conduc ing a i icial e iliza ion and applying
single-pai a he han mass spawning [41], and i pos-
sible implemen ing op imal con ibu ion selec ion [42,
43], o maximise gene ic gain while es ic ing he a e
o inb eeding. In cases whe e hese in e en ions a e no
su icien o inc ease Ne abo e he c i ical alue, ano he
op ion could be o in e change gene ic ma e ial om di -
e en gene ically imp o ed s ocks.
Supplemen a y In o ma ion
The online e sion con ains supplemen a y ma e ial a ailable a h ps:// doi.
o g/ 10. 1186/ s12711‑ 021‑ 00680‑9.
Addi ional ile1. Es ima es o Ne (loga i hmic scale) ac oss he las
100 gene a ions o each popula ion analysed. S aigh lines ep esen
es ima es ob ained using da a om pa en s and dashed lines ep esen
es ima es ob ained using da a om o sp ing.
Addi ional ile2. Es ima es o Ne (loga i hmic scale) ob ained wi h he LD
me hod o Hayes e al. [5] ac oss he las 100 gene a ions o each popula‑
ion analysed.
Addi ional ile3. Es ima es o Ne (loga i hmic scale) ob ained by com‑
pu e simula ions wi h he LD me hods o Hayes e al. [5] and San iago
e al. [6], using he so wa e SLiM3 [48].
Acknowledgemen s
The au ho s hank wo anonymous e e ees and he edi o s Helene Hayes,
Jack Dekke s and Na halie Saux‑Nogues o use ul commen s. They also g a e‑
ully acknowledge he compu ing ime g an ed by he Cen o de Supe ‑
compu ación de Galicia (CESGA) and o hei compu ing suppo on he
supe compu e Finis Te ae II ( 2.cesga.es).
Au ho s’ con ibu ions
MS pe o med he analyses and w o e he i s d a o he manusc ip . ES
and AC de eloped he me hod and so wa e used and con ibu ed o he
analyses. AF and EM‑G con ibu ed o he analyses. SC, PM, AM, CP, MK, MLA,
RH, MP, LB, TK, J‑SB, PH p o ided da a. BV and JF concei ed and designed he
s udy. AC ca ied ou he compu e simula ions and AC and MS analysed he
esul s. All au ho s con ibu ed o he discussion o esul s and he edi ion o
he e ised manusc ip . All au ho s ead and app o ed he inal manusc ip .
Funding
This wo k was suppo ed by he Eu opean Union’s Se en h F amewo k
P og amme (KBBE.2013.1.2‑659 10 unde G an Ag eemen No. 613611
FISHBOOST p ojec ), he Eu opean Commission Ho izon 2020 (H2020)
F amewo k P og amme h ough g an ag eemen no 727315 MedAID
p ojec (Medi e anean Aquacul u e In eg a ed De elopmen ), by Minis e io
de Ciencia e Inno ación (CGL2016‑75904‑C2), MCIN/AEI/h ps:// doi. o g/ 10.
13039/ 50110 00110 33 (PID2020‑114426GB‑C22 and PID2020‑114426GB‑C2),
Xun a de Galicia (GRC, ED431C 2020‑05) and Cen o singula de in es igación
de Galicia acc edi a ion 2019–2022, and he Eu opean Union (Eu opean
Regional De elopmen Fund—ERDF), Fondos Fede “Unha manei a de ace
Eu opa”. MK and MP we e also suppo ed by Minis y o Educa ion, You h and
Spo s o he Czech Republic—p ojec Biodi e zi y (CZ.02.1.01/0.0/0.0/16_
025/0007370). The Roslin Ins i u e was pa ly unded by Bio echnology and
Biological Sciences Resea ch Council Ins i u e S a egic P og amme g an s
(BBS/E/D/20241866, BBS/E/D/20002172 and BBS/E/D/20002174).
A ailabili y o da a and ma e ials
The aligned eads o ca p in he o ma o bam iles we e deposi ed in he
Na ional Cen e o Bio echnology In o ma ion (NCBI) eposi o y unde p ojec
ID PRJNA414021. Fo seabass, he sequence eads we e deposi ed a he NCBI
Sequence Read A chi e (SRA) unde he accession numbe PRJNA407892.
Decla a ions
E hics app o al and consen o pa icipa e
Tu bo da a we e ob ained in acco dance wi h he ecommenda ions o he
e hical egula ions and wi h he app o emen o Xun a de Galicia ( egis‑
e ed unde he code ES150730055401/16/PROD.VET.047ROD.01). Seabass
da a we e ob ained in acco dance wi h he ecommenda ions o ANSES/
ENVA/UPC no. 16, au ho ized by he “Minis è e de l’Educa ion Na ionale, de
l’Enseignemen Supé ieu e de la Reche che”, unde numbe 29/01/13‑5. The
app o al o he seab eam expe imen was aken om he Is i u o Zoop o ila ‑
ico Spe imen ale delle Venezie animal‑wel a e body and E hic commission
(Opinion no. 15/2013 o he 12 Sep embe 2013), au ho ized by he I alian
Minis y o Heal h (Law dec ee no. 135/2014‑B o he 28 h Ma ch 2014),
acco ding o Di ec i e 2010/63/EU on he p o ec ion o animals used o
scien i ic pu poses. Ca p da a we e ob ained in acco dance wi h he law on
he p o ec ion o animals agains c uel y (Ac No. 246/1992 Coll. o he Czech
Republic) and app o ed by Ins i u ional Animal Ca e and Use Commi ee
(IACUC).
Page 7 o 8
Sau ae al. Gene Sel E ol (2021) 53:85
Consen o publica ion
No applicable.
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Au ho de ails
1 Depa amen o de Mejo a Gené ica Animal, INIA‑CSIC, C a. de La Co uña,
km 7.5, 28040 Mad id, Spain. 2 Cen o de In es igación Ma iña, Facul ade de
Bioloxía, Uni e sidade de Vigo, 36310 Vigo, Spain. 3 Depa amen o de Biología
Funcional, Uni e sidad de O iedo, C/ Julián Cla e ía s/n, 33006 O iedo,
Spain. 4 CETGA, Clus e de Acuicul u a de Galicia, Pun a do Couso s/n,
15695 Aguiño‑Ribei a, Spain. 5 Geneaqua, 27002 Lugo, Spain. 6 Depa amen
o Zoology, Gene ics and Physical An h opology, Uni e sidade de San iago de
Compos ela, 27002 Lugo, Spain. 7 The Roslin Ins i u e and Royal (Dick) School
o Ve e ina y S udies, Uni e si y o Edinbu gh, Eas e Bush, Midlo hian EH25
9RG, UK. 8 Sou h Bohemian Resea ch Cen e o Aquacul u e and Biodi e si y
o Hyd ocenoses, Facul y o Fishe ies and P o ec ion o Wa e s, Uni e si y
o Sou h Bohemia in České Budějo ice, Zá iší 728/II, 389 25 Vodňany, Czech
Republic. 9 No ima AS, P.O. Box 210, 1431 Ås, No way. 10 Uni e si á degli S udi
di Pado a, Via 8 Febb aio 1848, 2, 35122 Pado a, PD, I aly. 11 And omeda G oup
SA, Leo . La iou 99, 190 02 Peania, G eece. 12 SYSAAF, S a ion LPGP/INRAE,
Campus de Beaulieu, 35042 Rennes, F ance. 13 Fe me Ma ine De Douhe , Rou e
du Douhe , 17840 La B ée‑les‑Bains, F ance.
Recei ed: 1 Feb ua y 2021 Accep ed: 22 Oc obe 2021
Re e ences
1. Hol sma k M, Kleme sdal G, Sonesson AK, Woolliams JA. Es ablishing a
base popula ion o a b eeding p og am in aquacul u e, om mul iple
subpopula ions, di e en ia ed by gene ic d i : I e ec s o he numbe
o subpopula ions, he i abili y and ma ing s a egies using op imum
con ibu ion selec ion. Aquacul u e. 2008;274:232–40.
2. Hol sma k M, Kleme sdal G, Sonesson AK, Woolliams JA. Es ablishing a
base popula ion o a b eeding p og am in aquacul u e, om mul iple
subpopula ions, di e en ia ed by gene ic d i : II sensi i i y o assump‑
ions on he addi i e gene ic ela ionships o base animals. Aquacul u e.
2008;274:241–6.
3. Fe nández J, To o MA, Sonesson AK, Villanue a B. Op imizing he c ea ion
o base popula ions o aquacul u e b eeding p og ams using pheno‑
ypic and genomic da a and i s consequences on gene ic p og ess. F on
Gene . 2014;5:e414.
4. Hill WG. Es ima ion o e ec i e popula ion size om da a on linkage
disequilib ium. Gene Res. 1981;38:209–16.
5. Hayes BJ, Vissche PM, McPa lan HC, Godda d ME. No el mul ilocus
measu e o linkage disequilib ium o es ima e pas e ec i e popula ion
size. Genome Res. 2003;13:635–43.
6. San iago E, No o I, Pa diñas AF, Sau a M, Wang J, Caballe o A. Recen
demog aphic his o y in e ed by high‑ esolu ion analysis o linkage
disequilib ium. Mol Biol E ol. 2020;37:3642–53.
7. Ma oso F, He mida M, Millán A, Blanco A, Sau a M, e al. Highly dense
linkage maps om 31 ull‑sibling amilies o u bo (Scoph ahlmus
maximus) p o ide insigh s in o ecombina ion pa e ns and ch omosome
ea angemen s h oughou a newly e ined genome assembly. DNA Res.
2018;25:439–50.
8. Aslam ML, Ca a o R, Bes in A, Ca iou S, Sonesson AK, B uan J‑S, e al.
Gene ics o esis ance o pho obac e iosis in gil head sea b eam (Spa us
au a a) using 2b‑RAD sequencing. BMC Gene . 2018;19:43.
9. Palaiokos as C, Ca iou S, Bes in A, B uan J‑S, Ha ay P, Mo in T, e al.
Genome‑wide associa ion and genomic p edic ion o esis ance o i al
ne ous nec osis in Eu opean sea bass (Dicen a chus lab ax) using RAD
sequencing. Gene Sel E ol. 2018;50:30.
10. Palaiokos as C, Robledo D, Vesely T, P chal M, Poko o a D, Piackno a V,
e al. Mapping and sequencing o a signi ican quan i a i e ai locus
a ec ing esis ance o Koi he pes i us in common ca p. G3 (Be hesda).
2018;8:3507–13.
11. B owning SR, B owning BL. Haplo ype phasing: exis ing me hods and
new de elopmen s. Na Re Gene . 2011;12:703–14.
12. Hill WG, Robe son A. Linkage disequilib ium in ini e popula ions. Theo
Appl Gene . 1968;38:226–31.
13. Oh a T, Kimu a M. Linkage disequilib ium due o andom gene ic d i .
Gene Res. 1969;13:47–55.
14. Sau a M, Tenesa A, Woolliams JA, Fe nández A, Villanue a B. E alua ion o
he linkage‑disequilib ium me hod o he es ima ion o e ec i e popu‑
la ion size when gene a ions o e lap: an empi ical case. BMC Genomics.
2015;16:922.
15. Waples RS, England PR. Es ima ing con empo a y e ec i e popula ion
size on he basis o linkage disequilib ium in he ace o mig a ion. Gene ‑
ics. 2011;189:633–44.
16. F ankham R, Ballou JD, B iscoe DA. In oduc ion o conse a ion gene ics.
Camb idge: Camb idge Uni e si y P ess; 2002.
17. F ankham R, B adshaw CJA, B ook BW. Gene ics in conse a ion manage‑
men : e ised ecommenda ions o he 50/500 ules, Red Lis c i e ia and
popula ion iabili y analyses. Biol Conse . 2014;170:56–63.
18. Caballe o A, B a o I, Wang J. Inb eeding load and pu ging: implica ions
o he sho ‑ e m su i al and he conse a ion managemen o small
popula ions. He edi y (Edinbu gh). 2017;118:177–85.
19. Waples RS, An ao T, Luika G. E ec s o o e lapping gene a ions on
linkage disequilib ium es ima es o e ec i e popula ion size. Gene ics.
2014;197:769–80.
20. B own TC, Woolliams JA, McAnd ew BJ. Fac o s in luencing e ec i e
popula ion size in comme cial popula ions o gil head seab eam, Spa us
au a a. Aquacul u e. 2005;247:219–25.
21. Bo ell V, Gallego V, Ga cía‑Fe nández C, Mazzeo I, Pé ez L, As u aino JF,
e al. Assessmen o pa en al con ibu ions o as ‑ and slow‑g owing
p ogenies in he sea b eam Spa us au a a L. using a new mul iplex PCR.
Aquacul u e. 2011;314:58–65.
22. Šeg ić‑Bubić T, G ubišić L, T umbić Ž, S anić R, Ljubko ić J, Ma šić‑Lučić
J, e al. Gene ic cha ac e iza ion o wild and a med Eu opean seabass
in he Ad ia ic sea: assessmen o a med escapees using a Bayesian
app oach. ICES J Ma Sci. 2017;74:369–78.
23. Ekna h A, Doyle RW. E ec i e popula ion size and a e o inb eeding in
aquacul u e o Indian majo ca ps. Aquacul u e. 1990;85:293–305.
24. Galla do JA, Ga cía X, Lho en e JP, Nei a R. Inb eeding and inb eeding
dep ession o emale ep oduc i e ai s in wo popula ions o Coho
salmon selec ed using BLUP p edic o s o b eeding alues. Aquacul u e.
2004;234:111–22.
25. Yáñez JM, Bassini LN, Filp M, Lho en e JP, Ponzoni R, Nei a R. Inb eeding
and e ec i e popula ion size in a coho salmon (Onco hynchus kisu ch)
b eeding nucleus in Chile. Aquacul u e. 2014;420:S15‑19.
26. Su G‑S, Liljedahl L‑E, Gall GAE. E ec s o inb eeding on g ow h and
ep oduc i e ai s in ainbow ou (Onco hynchus mykiss). Aquacul u e.
1996;142:139–48.
27. Pan e MA, Gje de B, McMillan I. E ec o inb eeding on body weigh
a ha es in ainbow ou , Onco hynchus mykiss. Aquacul u e.
2001;192:201–11.
28. Ba ía A, López ME, Yoshida G, Ca alhei o R, Lhho en e JP, Yáñez JM.
Popula ion genomic s uc u e and genome‑wide linkage disequilib ium
in a med A lan ic salmon (Salmo sala L.) using dense SNP geno ypes.
F on Gene . 2018;9:649.
29. Ba ía A, Ch is ensen KA, Yoshida G, Jedlicki A, Leong JS, Rondeau EB, e al.
Whole genome linkage disequilib ium and e ec i e popula ion size in a
coho Salmon (Onco hynchus kisu ch) b eeding popula ion using a high‑
densi y SNP a ay. F on Gene . 2019;10:498.
30. D’Amb osio J, Phocas F, Ha ay P, Bes in A, B a d‑Fudulea S, Ponce C,
e al. Genome‑wide es ima es o gene ic di e si y, inb eeding and e ec‑
i e size o expe imen al and comme cial ainbow ou lines unde going
selec i e b eeding. Gene Sel E ol. 2019;51:26.
31. Ponzoni RW, Khaw HL, Nguyen HN, Hamzah A. Inb eeding and e ec i e
popula ion size in he Malaysian nucleus o he GIFT s ain o Nile ilapia
(O eoch omis nilo icus). Aquacul u e. 2010;302:42–8.
32. do P ado FD, Ve a M, He mida M, Bouza C, Pa do BG, Vilas R, e al. Pa allel
e olu ion and adap a ion o en i onmen al ac o s in a ma ine la ish:
implica ions o ishe ies and aquacul u e managemen o he u bo
(Scoph halmus maximus). E ol Appl. 2018;11:1322–41.
33. Ga cía de León FJ, Chikhi L, Bonhomme F. Mic osa elli e polymo phism
and popula ion subdi ision in na u al popula ions o Eu opean sea bass
Dicen a chus lab ax (Linnaeus, 1758). Mol Ecol. 1997;6:51–62.
Page 8 o 8
Sau ae al. Gene Sel E ol (2021) 53:85
•
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•
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34. Louko i is D, Sa opolou E, Vogia zi E, Tsigenopoulos CS, Ko oulas G,
Magoulas A, e al. Gene ic a ia ion in a med popula ions o he gil head
sea b eam Spa us au a a in G eece using mic osa elli e DNA ma ke s.
Aquac Res. 2012;43:239–46.
35. Kohlmann K, Ke s en P. Gene ic a iabili y o Ge man and o eign com‑
mon ca p (Cyp inus ca pio L.) popula ions. Aquacul u e. 1999;173:435–45.
36. Kohlmann K, Ke s en P, Flajšhans M. Mic osa elli e‑based gene ic a i‑
abili y and di e en ia ion o domes ica ed, wild and e al common ca p
(Cyp inus ca pio L.) popula ions. Aquacul u e. 2005;247:253–66.
37. Janssen K, Cha anne H, Be en sen P, Komen H. Impac o selec i e b eed‑
ing on Eu opean aquacul u e. Aquacul u e. 2017;472:8–16.
38. Yoshida GM, Ba iá A, Co ea K, Cáce es G, Jedicki A, Cádiz MI, e al.
Genome‑wide pa e ns o popula ion s uc u e and linkage disequi‑
lib ium in a med Nile ilapia (O eoch omis nilo icus). F on Gene .
2019;10:745.
39. Kijas J, Ellio N, Kube P, E ans B, Bo w igh N, King H, e al. Di e si y and
linkage disequilib ium in a med Tasmanian A lan ic salmon. Anim Gene .
2017;48:237–41.
40. Glo e KA, Solbe g MF, McGinni y P, Hinda K, Ve spoo E, Coulson MW,
e al. Hal a cen u y o gene ic in e ac ion be ween a med and wild
A lan ic salmon: s a us o knowledge and unanswe ed ques ions. Fish
Fish. 2017;18:890–927.
41. Sonesson A, Ødegå d J. Ma ing s uc u es o genomic selec ion b eed‑
ing p og ams in aquacul u e. Gene Sel E ol. 2016;48:46.
42. Meuwissen THE. Maximizing he esponse o selec ion wi h a p ede ined
a e o inb eeding. J Anim Sci. 1997;75:934–40.
43. G undy B, Villanue a B, Woolliams JA. Dynamic selec ion p ocedu es o
cons ained inb eeding and hei consequences o pedig ee de elop‑
men . Gene Res. 1998;72:159–68.
44. Bouza C, He mida M, Pa do BG, Ve a M, Fe nández C, Fe nández C, e al.
An exp essed sequence ag (EST)‑en iched gene ic map o u bo
(Scoph halmus maximus): a use ul amewo k o compa a i e genomics
ac oss model and a med eleos s. BMC Gene . 2012;13:54.
45. Khul H, Sa opoulou E, Tine M, Ko oulas G, Magoulas A, Reinha d R. A
compa a i e BAC map o he gil head sea b eam (Spa us au a a L.). J
Biomed Bio echnol. 2011;2011:329025.
46. Chis iako DA, Tsigenopoulos CS, Lagnel J, Guo Y‑M, Hellemans, Haley
CS, e al. A combined AFLP and mic osa elli e linkage map and pilo
compa a i e genomic analysis o Eu opean sea bass Dicen a chus lab ax
L. Anim Gene . 2008;39:623–34.
47. Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y, e al. Genome sequence
and gene ic di e si y o he common ca p, Cyp inus ca pio. Na Gene .
2014;46:1212–9.
48. Halle BC, Messe PW. SLiM 3: o wa d gene ic simula ions beyond he
W igh –Fishe model. Mol Biol E ol. 2019;36:632–7.
Publishe ’s No e
Sp inge Na u e emains neu al wi h ega d o ju isdic ional claims in pub‑
lished maps and ins i u ional a ilia ions.