Ca dosoe al. Gene Sel E ol (2018) 50:56
h ps://doi.o g/10.1186/s12711-018-0425-7
RESEARCH ARTICLE
Pa e ns o homozygosi y ininsula
andcon inen al goa b eeds
Taina F. Ca doso1,2†, Ma cel Amills1,3*† , F ancesca Be olini4, Max Ro hschild4, Gab iele Ma as5, Gee Boink6,
Jo di Jo dana3, Juan Capo e7, Sean Ca olan8, Jón H. Hallsson9, Juha Kan anen10, Agueda Pons11,
Johannes A. Lens a12* and The Adap Map Conso ium
Abs ac
Backg ound: Gene ic isola ion o b eeds may esul in a signi ican loss o di e si y and ha e consequences on
heal h and pe o mance. In his s udy, we examined he e ec o geog aphic isola ion on cap ine gene ic di e si y
pa e ns by geno yping 480 indi iduals om 25 Eu opean and A ican b eeds wi h he Goa SNP50 BeadChip and
compa ing pa e ns o homozygosi y o insula and nea by con inen al b eeds.
Resul s: Among he b eeds analysed, numbe and o al leng h o ROH a ied conside ably and depending on
b eeds, ROH could co e a subs an ial ac ion o he genome (up o 1.6 Gb in Icelandic goa s). When compa ed wi h
hei con inen al coun e pa s, goa s om Iceland, Madagasca , La Palma and I eland (Bilbe y and A an) displayed a
signi ican inc ease in ROH co e age, ROH numbe and FROH alues (P alue < 0.05). Goa s om Medi e anean islands
ep esen a mo e complex case because ce ain popula ions displayed a signi ican ly inc eased le el o homozygo‑
si y (e.g. Gi gen ana) and o he s did no (e.g. Co se and Sa da). Co ela ions o numbe and o al leng h o ROH o
insula goa popula ions wi h he dis ance be ween islands and he nea es con inen al loca ions e ealed an e ec o
ex emely long dis ances on he pa e ns o homozygosi y.
Conclusions: These esul s indica e ha he e ec s o insula iza ion on he pa e ns o homozygosi y a e a iable.
Goa s aised in Madagasca , Iceland, I eland (Bilbe y and A an) and La Palma, show high le els o homozygosi y,
whe eas hose b ed in Medi e anean islands display pa e ns o homozygosi y ha a e simila o hose ound in
con inen al popula ions. These esul s indica e ha he di e si y o insula goa popula ions is modula ed by mul iple
ac o s such as geog aphic dis ibu ion, popula ion size, demog aphic his o y, ading and b eed managemen .
© The Au ho (s) 2018. 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
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Backg ound
The ad en o nex -gene a ion sequencing and high
h oughpu geno yping echniques has made i possible
o iden i y, in he genomes o mul iple species, con inu-
ous homozygous s e ches o sequence, which a e named
uns o homozygosi y (ROH) [1]. The genomic dis i-
bu ion, abundance, and leng h o ROH a e modula ed
by mul iple ac o s including local ecombina ion a e,
guanine-cy osine con en , posi i e selec ion and demog-
aphy [2, 3]. A high equency o long ROH is o en
caused by ecen inb eeding, whe eas a high equency
o sho ROH can be explained by he occu ence o an
ancien ounde e ec o popula ion bo leneck. A e
he i s pionee ing s udy o Fe enčako ić e al. [4], he
pa e ns o ROH ha e been cha ac e ized o mul iple
domes ic species and b eeds wi h he goal o making
in e ences abou hei his o y and demog aphy as well as
o iden i ying he genomic oo p in o na u al and a i i-
cial selec ion [5].
Geog aphic isola ion o popula ions may lead o a
conside able loss o di e si y, an inc ease in inb eeding
and ulne abili y o s ochas ic e en s [6]. Fo ins ance,
human popula ions wi h a his o y o p olonged
Open Access
G
ene ics
S
elec ion
E olu ion
*Co espondence: ma cel[email p o ec ed]; j[email p o ec ed]
†Taina F. Ca doso and Ma cel Amills sha e he i s au ho ship
1 Depa men o Animal Gene ics, Cen e o Resea ch in Ag icul u al
Genomics (CRAG), CSIC‑IRTA‑UAB‑UB, Campus de la Uni e si a
Au ònoma de Ba celona, 08193 Bella e a, Ba celona, Spain
12 Facul y o Ve e ina y Medicine, U ech Uni e si y, U ech , The
Ne he lands
Full lis o au ho in o ma ion is a ailable a he end o he a icle
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Ca dosoe al. Gene Sel E ol (2018) 50:56
isola ion on he O kney o Dalma ian Islands o in Sa -
dinia ha e longe ROH han con inen al popula ions,
which indica es an ele a ed ela edness [7, 8]. A high
equency o ROH can ha e de imen al e ec s on bio-
logical i ness and ep oduc i e success because ROH
a e o en en iched in dele e ious mu a ions [9]. Indeed,
mi ochond ial encephalomyopa hy is ela i ely e-
quen in people om he Fa oe Islands due o homozy-
gosi y o he SUCLA2 gene [10]. In ca le, Zhang e al.
[11] epo ed ha dele e ious a ia ions a e o e ep-
esen ed in ROH egions, pa icula ly in hose longe
han 3 Mbp. Howe e , geog aphically isola ed popu-
la ions may ha e e ained ancien alleles o a ian s
ha a e no ound in o he popula ions [12, 13], which
e lec s adap a ion o ha sh en i onmen s and/o a
p ac ice o b eed managemen ha a e no common o
mainland popula ions [13–15].
Recen ly, genome-wide single nucleo ide polymo -
phism (SNP) da a o a comp ehensi e panel o goa s
b eeds has become a ailable [16]. Fo he same panel
o b eeds, signa u es o selec ion [17] and he e ec s o
popula ion size, b eed managemen and c ossb eeding
on he pa e ns o ROH as well as ch omosomal ROH
ho spo s ha e been epo ed [18]. The aim o ou s udy
was o in es iga e i goa b eeds ha a e aised in islands
ha e highe le els o homozygosi y han hei con inen al
coun e pa s. In o de o achie e his goal, we compa ed
he numbe and genomic co e age o ROH in 25 cap ine
b eeds om 16 Eu opean and A ican islands wi h hose
o nine con inen al popula ions.
Me hods
Goa sampling andgeno yping
Goa s we e sampled and geno yped as pa o he Adap -
Map p ojec [19] and see Table1. The geog aphic dis-
ibu ion o he b eeds in es iga ed in his s udy is
illus a ed in Figu eS1 (see Addi ional ile1: Figu eS1).
Genomic DNA was ex ac ed wi h s anda d p o o-
cols and goa s we e geno yped wi h he Illumina Goa
SNP50 BeadChip [20] by ollowing he manu ac u e ’s
ins uc ions. Monomo phic and unmapped SNPs in
he whole da ase , and SNPs wi h a call a e lowe han
98% we e elimina ed. Indi iduals wi h a geno ype call
a e lowe han 96% we e emo ed. Quali y con ol was
pe o med by using he PLINK p og am [21]. The inal
da ase included 46,654 SNPs and 480 goa s wi h 260
and 220 indi iduals om insula and con inen al popu-
la ions, espec i ely (Table1) and (see Addi ional ile1:
Figu eS1). In o de o calcula e allele-sha ing dis ances
(ASD), linkage disequilib ium-p uning o SNPs was
implemen ed (plink op ion—indep-pai wise 50 5 0.03)
[21], which e ained 19,879 SNPs.
Da a analysis
The Zana di so wa e [22] was used o iden i y ROH. Runs
o homozygosi y we e de ined as homozygous genomic
s e ches ha a e a leas 1Mb long and ha con ain a min-
imum numbe o 15 SNPs. We allowed one he e ozygous
SNP pe ROH o accoun o geno yping e o s. Coo di-
na es o p incipal componen analysis (PCA) and allele-
sha ing dis ances (ASD) we e calcula ed wi h he PLINK
p og am [21]. A neighbo -joining ee was buil and isual-
ized wi h he Spli s ee p og am [23].
Genomic inb eeding de i ed om ROH co e age (FROH)
was calcula ed by di iding o al ROH leng h pe indi-
idual by o al genome leng h ac oss all 29 au osomes
(2456.50Mb). Inb eeding coe icien s i.e. Fhe , Fha 1, Fha 2,
and Fha 3 we e calcula ed wi h he PLINK so wa e [21] o
popula ions wi h a leas 20 indi iduals. On he one hand,
he—he command o PLINK [21] was used o compu e
obse ed and expec ed au osomal homozygous geno ype
coun s (Fhe ) and on he o he hand, we used he—ibc com-
mand o PLINK [21] o calcula e Fha , Fha 2 and Fha 3 pa am-
e e s. Obse ed he e ozygosi y (Ho) and e ec i e size (Ne)
pa ame e s we e e ie ed om es ima es p o ided by
Colli and cowo ke s [16].
S a is ical analyses we e pe o med by using he R so -
wa e .2.15.3 [24]. The alues and s a is ical signi icances
o Spea man’s ank co ela ions (ρ) o FROH wi h Ho and Ne
we e compu ed. We also calcula ed Spea man’s ank co -
ela ions (ρ) o numbe and o al leng h o ROH o insula
goa popula ions wi h he dis ance be ween each island and
he nea es con inen al loca ion.
We used a gene alized leas squa es model implemen ed
in he nlme package (R so wa e .2.15.3, [24]) o in e
whe he FROH and o al ROH leng h and numbe di e ed
signi ican ly be ween con inen al and insula popula-
ions. We conside ed six g oups o b eeds and pe o med
s a is ical compa isons be ween he b eeds con ained
wi hin each g oup (all b eeds agains each o he wi hin
each g oup). We did no pe o m s a is ical compa isons
be ween g oups o be ween b eeds belonging o di e -
en g oups. The ollowing g oups o b eeds we e aken
in o conside a ion: (1) Icelandic goa s, Danish, Du ch and
Finnish Land ace; (2) A an, Bilbe y, Mul anny, and Fos-
ses; (3) A gen a a, Asp omon ana, Ciocia a G igia, Co se,
Gi gen ana, Mal ese Sa da and Sa da; (4) Mallo quina and
Blanca de Rasque a; (5) Mo occan goa and Palme a; and
(6) And oy, Diana, Menabe, Ma ebele, So ia and SudOues .
On he basis o explo a o y analyses o he da a ( esul s no
shown), we used a model which assumes inequali y o he
a iances (he e oscedas ici y) ha a e associa ed wi h each
o he h ee pa ame e s aken in o conside a ion (FROH and
o al ROH leng h and numbe ) and each popula ion:
Y
i=Xiβ+εi,εi∼N

0, σ2i

and i=1, ...,m
,
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Ca dosoe al. Gene Sel E ol (2018) 50:56
whe e
β
is a ec o o he ixed e ec “b eed” (m le els),
Xi
is an incidence ma ix ela ing
Yi
o
β
, and
i
is a pos-
i i e-de ini e ma ix o he a iances and co a iances o
he wi hin-g oup e o s. Fo ull de ails on he me hodol-
ogy, see Pinhei o and Ba es [25]. The leas squa e means
o each pa ame e and popula ion we e con as ed on a
pai wise basis wi h a Wald uni a ia e es o signi icance
[26] and mul iple es ing was adjus ed wi h he Bon e -
oni co ec ion.
Resul s
Ou panel o goa b eeds included insula b eeds om
di e en egions (see Addi ional ile1: Figu eS1): Ice-
land (N = 11) and I eland (N = 31) in no he n Eu ope;
Co sica (N = 29), Sa dinia (N = 39), Sicily (N = 48) and
Mallo ca (N = 18) in Sou he n Eu ope; and La Palma
(N = 15) and Madagasca (N = 69) in A ica. Each o
hese was compa ed o he nea es con inen al popu-
la ions. Among he con inen al popula ions, he Finn-
ish, Danish and Du ch goa s belong o he No dic ype
and a e also subjec o gene ic isola ion ei he because
hey a e b ed on a peninsula (Finland, Denma k) o
managed unde he scope o a s ic ly closed he dbook
(Ne he lands). The PCA i s ac o ial map is shown in
Fig.1a. The i s wo coo dina es PC1 and PC2 high-
ligh he sepa a ion be ween Malagasy and Icelandic
goa s, espec i ely. These wo b eeds and he goa pop-
ula ions om La Palma and Iceland, also ha e ex eme
posi ions on he PC1-PC3 and PC1-PC4 plo s (see
Addi ional ile2: Figu e S2), bu his was no obse ed
Table 1 ROH numbe , ROH leng h andFROH mean, minimum (min) andmaximum (max) alues calcula ed o  he25 goa
popula ions used in his s udy (SE = s anda d e o )
B eed code B eed name Coun y Numbe
o animals ROH leng h ROH numbe FROH
Mean ± SE Min/max Mean ± SE Min/max Mean ± SE Min/max
AND And oy Madagasca 6 478.44 ± 19.43 423.28/559.05 259.67 ± 7.88 235/289 0.19 ± 0.01 0.17/0.23
ARG A gen a a I aly (Sicily) 24 47.01 ± 9.21 16.78/248.58 21.79 ± 1.15 13/35 0.02 ± 0.00 0.01/0.10
ARR A an I eland 8 733.63 ± 47.82 513.01/938.65 178.00 ± 7.05 147/209 0.30 ± 0.02 0.21/0.38
ASP Asp omon ana I aly 23 135.05 ± 30.77 20.77/599.81 35.61 ± 4.40 15/102 0.05 ± 0.01 0.01/0.24
BLB Bilbe y I eland 10 533.28 ± 44.00 88.00/780.21 67.00 ± 5.33 23/114 0.22 ± 0.02 0.04/0.32
CCG Ciocia a G igia I aly 16 155.39 ± 29.90 7.83/362.79 30.63 ± 4.12 7/60 0.06 ± 0.01 0.00/0.15
CRS Co se F ance (Co ‑
sica) 29 93.72 ± 14.29 23.55/295.13 34.86 ± 1.68 18/65 0.04 ± 0.01 0.01/0.12
DIA Diana Madagasca 14 636.87 ± 60.53 481.75/1279.29 265.79 ± 4.88 229/292 0.26 ± 0.02 0.20/0.52
DKL Danish Lan‑
d ace Denma k 50 401.18 ± 28.00 490.30/714.81 67.06 ± 1.94 111/141 0.16 ± 0.01 0.20/0.29
DUL Du ch Lan‑
d ace Ne he lands 15 622.60 ± 15.80 133.11/889.28 125.27 ± 1.96 41/102 0.25 ± 0.01 0.05/0.36
FIN Finnish Lan‑
d ace Finland 20 225.46 ± 32.00 118.47/686.10 80.75 ± 2.77 65/122 0.09 ± 0.01 0.05/0.28
FSS Fosses F ance 24 218.30 ± 42.49 25.07/665.76 47.46 ± 3.69 15/79 0.09 ± 0.02 0.01/0.27
GGT Gi gen ana I aly (Sicily) 24 363.58 ± 37.61 161.21/863.58 93.71 ± 2.60 73/122 0.15 ± 0.02 0.07/0.35
ICL Icelandic goa s Iceland 11 1625.59 ± 57.30 1263.82/1979.66 366.45 ± 12.60 324/455 0.66 ± 0.02 0.51/0.81
MAL Mallo quina Spain (Mal‑
lo ca) 18 334.68 ± 63.06 49.57/938.51 74.39 ± 4.61 29/102 0.14 ± 0.03 0.02/0.38
MEN Menabe Madagasca 19 797.36 ± 21.95 673.26/1156.91 392.63 ± 4.70 345/425 0.32 ± 0.01 0.27/0.47
MLS Mal ese Sa da I aly (Sa dinia) 12 287.56 ± 36.34 24.37/486.45 73.42 ± 6.71 18/102 0.12 ± 0.01 0.01/0.20
MOR Mo occan goa Mo occo 30 151.03 ± 40.45 15.76/1025.09 32.43 ± 2.94 13/74 0.06 ± 0.02 0.01/0.42
MTB Ma ebele Zimbabwe 22 146.35 ± 14.97 110.73/451.20 84.55 ± 1.37 71/96 0.06 ± 0.01 0.05/0.18
MUL Mul anny I eland 13 323.02 ± 33.76 59.55/604.71 74.50 ± 5.42 36/111 0.13 ± 0.01 0.02/0.25
PAL Palme a Spain (La
Palma) 15 571.80 ± 14.11 471.68/641.05 276.13 ± 4.86 234/314 0.23 ± 0.01 0.19/0.26
RAS Blanca de
Rasque a Spain 20 246.55 ± 37.98 20.01/588.65 56.45 ± 5.33 17/103 0.10 ± 0.02 0.01/0.24
SAR Sa da I aly (Sa dinia) 27 97.19 ± 17.14 21.52/376.47 34.81 ± 2.35 14/55 0.04 ± 0.01 0.01/0.15
SOF So ia Madagasca 22 854.77 ± 30.68 672.20/1251.19 363.95 ± 4.65 310/391 0.35 ± 0.01 0.27/0.51
SOU SudOues Madagasca 8 564.73 ± 16.40 488.34/637.01 300.63 ± 7.40 263/325 0.23 ± 0.01 0.20/0.26
Page 4 o 11
Ca dosoe al. Gene Sel E ol (2018) 50:56
o goa s om Sou he n Eu opean islands (Mallo ca,
Co sica, Sa dinia and Sicily).
A neighbo -joining ee o ASD dis ances (Fig. 1b)
shows a clea clus e ing o goa s om he same b eed,
excep o wo Mal ese Sa da goa s ha clus e wi h he
Sa da and ice e sa. Gi gen ana, Palme a and So ia a e
nes ed wi hin he Asp omon ana, Mo occo and Diana
popula ions, espec i ely, while bo h Menabe and Sud-
Oues popula ions a e wi hin he And oy popula ion.
Mos b eeds appea o be homogeneous, excep o Dan-
ish Land ace, Mallo quina and Asp omon ana, which
show some he e ogenei y. Fo Icelandic, I ish, Palme a
and Malagasy goa s, we obse ed a dec ease in gene ic
dis ances be ween indi iduals om he same b eed
(Fig.1b) bu no o goa s om Medi e anean islands.
Apa om he ex emely inb ed Icelandic goa s [12],
gene ic isola ion was mos in ense o he I ish A an,
Du ch, Palme an (Cana y Islands) and Malagasy (And oy,
So ia, Diana, Menabe and Sud-Oues ) popula ions. As
shown in Figu e S3 (see Addi ional ile3: Figu eS3), he
wi hin-b eed ASD dis ances co ela e closely wi h Ho,
which indica es ha a ee as ha shown in Fig.1b ai h-
ully illus a es he di e si y pa e ns and a he same
ime ep oduces he egional clus e ing o b eeds [16].
The numbe o ROH and he o al ROH co e age a e
displayed in Fig.2 and he means and s anda d e o s o
hese wo pa ame e s a e in Fig.3 and Table1. Signi ican
di e ences in ROH co e age, ROH numbe and FROH
(Padj- alue < 0.05) we e obse ed be ween goa s om
Iceland, Madagasca , La Palma and I eland (Bilbe y and
A an) and hei con inen al coun e pa s (Fig.3). Goa s
om Medi e anean islands ep esen a mo e complex
case because ce ain popula ions display a signi ican ly
inc eased le el o homozygosi y (e.g. Gi gen ana) while
o he s do no (e.g. Co se and A gen a a).
Genomic ROH co e age is di ec ly p opo ional o he
ROH-based inb eeding coe icien s [27] ha a e shown
in Fig.4 and Table1. In he Icelandic, A an (I eland),
Malagasy and Palme an goa popula ions, he numbe
o ROH and hei o al leng h ange om 147 o 455 and
om 423.28 o 1979.66Mb (Fig.4 and Table1), espec-
i ely, which co espond o ex emely high inb eeding
coe icien s in Icelandic (FROH = 0.66), and Malagasy
goa s (FROH = 0.19–0.35). The gene ic isola ion o he
Du ch goa s [14] is e idenced by a high ROH co e age
anging om 133.11 o 889.28Mb (FROH = 0.25) a he
han by he numbe o ROH (41–102). Inb eeding coe -
icien s a e also high o he Palme an (FROH = 0.23), Bil-
be y (FROH = 0.22) and A an (FROH = 0.30) popula ions
(Fig.4 and Table1). In con as , Medi e anean insula
goa s ha e a mos 122 ROH wi h a mean o al leng h o
47.1–363.6Mb (Fig.2 and Table1), hese alues being
simila o hose obse ed o nea by con inen al goa
popula ions (Fig.3). A o al leng h o ROH g ea e han
500Mb was obse ed only o a ew Gi gen ana and Mal-
lo quina goa s.
Fig. 1 a PCA plo o indi iduals om 25 insula o con inen al popula ions. Red and da k blue indica e insula and con inen al b eeds, espec i ely,
wi h a high le el o homozygosi y. Pink and ligh blue indica e insula and con inen al b eeds, espec i ely, wi h a low o mode a e le el o
homozygosi y. b Neighbo ‑joining ee based on allele‑sha ing dis ances ep esen ing he gene ic ela ionships among insula and con inen al
goa popula ions
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Ca dosoe al. Gene Sel E ol (2018) 50:56
Fig. 2 Numbe and o al leng h o ROH in A ican, Eu opean and Medi e anean insula and con inen al goa popula ions. Red and da k blue
indica e insula and con inen al b eeds, espec i ely, wi h a high le el o homozygosi y. Pink and ligh blue indica e insula and con inen al b eeds,
espec i ely, wi h a low o mode a e le el o homozygosi y. The numbe o ROH ound o each indi idual genome (y‑axis) is plo ed agains o al
ROH size (i.e. numbe o Mb co e ed by ROH in each genome, x‑axis). The ollowing codes a e used (insula popula ions in bold): AND, And oy
(Madagasca ); ARG, A gen a a (Sicily); ARR, A an (I eland); ASP, Asp omon ana; BLB, Bilbe y (I eland); CCG, Ciocia a G igia; CRS, Co se (Co sica);
DIA, Diana (Madagasca ); DKL, Danish Land ace; DUL, Du ch Land ace; FIN, Finnish Land ace; FSS, Fosses; GGT, Gi gen ana (Sicily); ICL, Icelandic
goa s (Iceland); MAL, Mallo quina (Mallo ca); MEN, Menabe (Madagasca ); MLS, Mal ese Sa da (Sa dinia); MOR, Mo occan goa ; MTB, Ma ebele;
MUL, Mul anny (I eland); PAL, Palme a (La Palma); RAS, Blanca de Rasque a; SAR, Sa da (Sa dinia); SOF, So ia (Madagasca ); SOU, SudOues
(Madagasca )
Fig. 3 S a is ical analysis o he mean ROH numbe s, ROH co e age and FROH. Red and da k blue indica e insula and con inen al b eeds,
espec i ely, wi h high homozygosi y. Pink and ligh blue indica e insula and con inen al b eeds, espec i ely, wi h low o modes homozygosi y.
Di e en le e s indica e s a is ically signi ican di e ences be ween g oups (mean ± s anda d e o , linea models wi h he e oscedas ic wi hin
g oup‑e o s, Padj‑ alue < 0.05). The ollowing codes a e used (insula popula ions in bold): AND, And oy (Madagasca ); ARG, A gen a a (Sicily);
ARR, A an (I eland); ASP, Asp omon ana; BLB, Bilbe y (I eland); CCG, Ciocia a G igia; CRS, Co se (Co sica); DIA, Diana (Madagasca ); DKL, Danish
Land ace; DUL, Du ch Land ace; FIN, Finnish Land ace; FSS, Fosses; GGT, Gi gen ana (Sicily); ICL, Icelandic goa s (Iceland); MAL, Mallo quina
(Mallo ca); MEN, Menabe (Madagasca ); MLS, Mal ese Sa da (Sa dinia); MOR, Mo occan goa ; MTB, Ma ebele; MUL, Mul anny (I eland); PAL,
Palme a (La Palma); RAS, Blanca de Rasque a; SAR, Sa da (Sa dinia); SOF, So ia (Madagasca ); SOU, SudOues (Madagasca )
(See igu e on nex page.)

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Ca dosoe al. Gene Sel E ol (2018) 50:56
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Ca dosoe al. Gene Sel E ol (2018) 50:56
In mos b eeds, we ound an in e se ela ionship
be ween ROH size and equency (Fig.5). Howe e , ROH
longe han 1–5Mb a e ela i ely equen in he genome
o Icelandic, I ish, Du ch, Danish and Mallo quina goa s.
Fo he ex emely inb ed Iceland goa , an a e age o
366 ROH we e de ec ed, 286 o which we e longe han
1 o5Mb. We also in es iga ed he ela ionship be ween
FROH and se e al popula ion pa ame e s including (Ho,
Ne and he inb eeding coe icien s Fhe , Fha 1, Fha 2 and
Fha 3 calcula ed wi h PLINK [21] i.e. (see Addi ional
ile4: TableS1 and Addi ional ile5: TableS2). On he
one hand, Spea man co ela ions coe icien s be ween
FROH and Ne and Ho we e nega i e (ρ < − 0.87) and sig-
ni ican (P alue < 0.002), which e lec s ha popula ions
wi h smalle Ne unde go mo e gene ic d i han la ge
popula ions [27] and, in consequence, hey end o be
mo e homozygous. On he o he hand, Spea man co e-
la ions coe icien s be ween FROH and he ou inb eed-
ing coe icien s calcula ed wi h PLINK [21] we e posi i e
(ρ < 0.64–0.88) and signi ican (P alue < 0.01) o e y sig-
ni ican (P alue < 0.0001). P e ious s udies ha e epo ed
simila ends o co ela ions be ween FROH and a wide
ange o inb eeding coe icien s [27–29].
We also calcula ed Spea man co ela ions coe icien s
o ROH leng h and numbe wi h he dis ance o insu-
la goa popula ions o he nea es con inen al coas al
si e. Fo goa s aised in dis an islands, such as Ice-
land (1277km om No way) o Madagasca (1051km
Fig. 4 Plo o he ac ion o he genome co e ed by ROH (FROH) in insula ( ed) and con inen al (blue) goa popula ions. The ollowing codes a e
used (insula popula ions in bold): AND, And oy (Madagasca ); ARG, A gen a a (Sicily); ARR, A an (I eland); ASP, Asp omon ana; BLB, Bilbe y
(I eland); CCG, Ciocia a G igia; CRS, Co se (Co sica); DIA, Diana (Madagasca ); DKL, Danish Land ace; DUL, Du ch Land ace; FIN, Finnish Land ace;
FSS, Fosses; GGT, Gi gen ana (Sicily); ICL, Icelandic goa s (Iceland); MAL, Mallo quina (Mallo ca); MEN, Menabe (Madagasca ); MLS, Mal ese Sa da
(Sa dinia); MOR, Mo occan goa ; MTB, Ma ebele; MUL, Mul anny (I eland); PAL, Palme a (La Palma); RAS, Blanca de Rasque a; SAR, Sa da (Sa dinia);
SOF, So ia (Madagasca ); SOU, SudOues (Madagasca )
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Ca dosoe al. Gene Sel E ol (2018) 50:56
om Mozambique), ROH numbe and o al leng h had
he la ges alues. Spea man co ela ion coe icien s o
he dis ances wi h ROH numbe (ρ = 0.54 and, P alue
= 0.023) and o al leng h (ρ = 0.63 and, P alue = 0.007)
we e posi i e and signi ican .
Discussion
In insula and o he isola ed popula ions, homozygosi y
is o en inc eased by ounde e ec s and geog aphic iso-
la ion. In ou s udy, he la ge numbe s and longe o al
leng hs o ROH and highe FROH in goa s om Iceland,
I eland, La Palma and Madagasca han in hei con i-
nen al coun e pa s illus a e his inc ease in he le el
o homozygosi y (Table1 and Figs.2, 3 and 4). In con-
as , Medi e anean insula and con inen al popula-
ions o m a igh clus e . Al hough goa popula ions ha
a e aised in emo e islands end o ha e highe le els
o homozygosi y, o he ac o s a e also in ol ed, such
as b eed managemen , his o y and demog aphy, which
could ha e s ong e ec s on b eed di e si y. We we e
no able o analyse he impac o some o hese ac o s
because o lack o in o ma ion (his o ic and demog aphic
eco ds a e sca ce o comple ely absen o mos o he
b eeds unde analysis).
The analysis illus a ed in Fig. 1a e eals a s ong
sepa a ion be ween Malagasy and Ma ebele (Zimba-
bwe) and be ween Icelandic and No dic Land ace goa
popula ions and, o a lesse ex en , be ween Palme an
and Mo occan goa s. This esul p obably e lec s he
ex eme geog aphic isola ion o hese h ee insula pop-
ula ions. Indeed, we ound ha ROH numbe and o al
leng h we e co ela ed posi i ely wi h dis ance be ween
each island and he nea es con inen al loca ion. E ec s
o insula iza ion and/o small e ec i e popula ions sizes
Fig. 5 Dis ibu ion o ROH acco ding o hei size in A ican, Eu opean and Medi e anean insula and con inen al goa popula ions. The ollowing
codes a e used (insula popula ions in bold): AND, And oy (Madagasca ); ARG, A gen a a; ARR, A an (I eland); ASP, Asp omon ana; BLB, Bilbe y
(I eland); CCG, Ciocia a G igia; CRS, Co se (Co sica); DIA, Diana (Madagasca ); DKL, Danish Land ace; DUL, Du ch Land ace; FIN, Finnish Land ace;
FSS, Fosses; GGT, Gi gen ana (Sicily); ICL, Icelandic goa s (Iceland); MAL, Mallo quina (Mallo ca); MEN, Menabe (Madagasca ); MLS, Mal ese Sa da
(Sa dinia); MOR, Mo occan goa ; MTB, Ma ebele; MUL, Mul anny (I eland); PAL, Palme a (La Palma); RAS, Blanca de Rasque a; SAR, Sa da (Sa dinia);
SOF, So ia (Madagasca ); SOU, SudOues (Madagasca )
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Ca dosoe al. Gene Sel E ol (2018) 50:56
we e p e iously epo ed in a compa ison be ween Japa-
nese wild boa s and Asian mainland pigs [2], and o se -
e al insula and/o inb ed ca le popula ions [28].
We obse ed he mos ex eme combined e ec s o
ounde e en s, geog aphic isola ion and small popu-
la ion size o he Icelandic goa s wi h 324 o455 ROH
ha co e be ween 1263 and 1979Mb, a high equency
o e y long ROH (> 30 Mb) and a e y high FROH o
0.66 (Table1 and Figs.3, 4, 5). Icelandic goa s ha e a
No h-Eu opean (mos likely No wegian) o igin and
we e impo ed du ing he coloniza ion o Iceland o e
1100yea s ago [12, 29]. The lack o e idence o subse-
quen goa impo a ions sugges s a scena io o s ong
geog aphic isola ion. Mo eo e , he e we e less han 100
Icelandic goa s a he end o he nine een h cen u y and
again in 1960, bu , in 1994, he es ima ed census was
equal o 348 heads dis ibu ed o e 48 locks [29]. Small
popula ion size combined wi h a agmen ed dis ibu-
ion p obably a ou ed he main enance o high le els
o inb eeding in his goa popula ion. Old I ish goa s,
mos no ably hose om A an and Bilbe y, also show
inc eased ROH co e age, bu no as ex eme as ha
obse ed in Icelandic goa s (Figs.3, 4, 5). The ex emely
small popula ion (27 in 2006, [30]) o Bilbe y goa s has
led o he eme gence o ela i ely long ROH (Figs.3, 5),
which indica es ecen consanguini y. Old I ish goa s
ha e been subjec ed o casual hun ing and indisc imina e
culling o e al he ds, which has led his popula ion o he
e ge o ex inc ion [31].
Inc eased homozygosi y was also obse ed in goa
popula ions ha ha e la ge popula ion sizes bu , as
o he Icelandic and I ish goa s, ha e endu ed a p o-
longed geog aphic isola ion. Fo bo h Palme a and
Malagasy goa s, a ela i ely la ge numbe o ROH, high
ROH co e age (Fig.2) and ele a ed FROH (0.19–0.35,
Table1) we e ound, bu sho ROH (1–5Mb) we e
p edominan (Fig.5). This is p obably he consequence
o an ancien ounde e ec and geog aphic isola-
ion, whe eas hei la ge popula ion size (1.2 million
in Madagasca and mo e han 6000 in La Palma) p e-
en s consanguini y and he gene a ion o long ROH.
Madagasca , he ou h la ges island in he wo ld, was
se led by Aus onesians, who a i ed om Bo neo
du ing he i h o se en h cen u ies, and subsequen ly
by Ban u people [32], bu i is clea ha Malagasy goa s
a e o A ican o igin (Fig. 1). The pa e ns o ROH
obse ed in ou s udy sugges ha , a e an ini ial
ounde e ec , Malagasy goa s we e subjec o a his o y
o p olonged geog aphic isola ion, wi h he dis ance o
1000km be ween Madagasca and he A ican land-
mass cons i u ing an e ec i e ba ie o gene low. La
Palma, in he Cana ian a chipelago, was se led 2500
YBP by colonis s wi h p obably a Be be ances y and
emained isola ed om he main ma i ime ou es un il
i s coloniza ion by he Spanish in he i een h cen u y
[33]. This No h A ican ances y o Palme an goa s is
e lec ed in he neighbo -joining ee shown in Fig.1,
wi h Palme an goa s displaying a close ela ionship
wi h Mo occan goa s. In he La Palma island, a limi ed
numbe o ounde s in combina ion wi h geog aphic
isola ion esul ed in a low le el o di e si y o cap ine
m DNA [34] and a high ROH co e age.
The abo e esul s a e in s ong con as wi h he majo -
i y o he Medi e anean insula goa b eeds showing
ROH pa e ns and FROH alues ha a e simila o hose
obse ed in nea by con inen al popula ions (Table1 and
Figs.2, 3, 4, 5). Mallo ca, Co sica, Sicily and Sa dinia a e
ela i ely close (5–300km) o con inen al Eu ope and a e
loca ed along ma i ime ou es ha we e used in ensi ely
by he Phoenicians, Ca haginians, G eeks, Romans,
A abs and many o he sea a ing ci iliza ions [35]. This
si ua ion p obably a ou ed he ecu en admix u e o
goa popula ions wi h di e en gene ic backg ounds,
hus coun e ac ing he dec ease in gene ic a ia ion p o-
duced by he ini ial ounde e ec . This is also illus a ed
by he seg ega ion o he m DNA G haplog oup in Mal-
lo quina goa s, which so a has only been iden i ied in
goa s om Egyp , I an and Tu key [34]. Fu he mo e, a
mixed ances y wi h a majo in luence o Mal ese goa s
has been men ioned o Sa da goa [36]. Howe e , Mal-
lo quina and Gi gen ana goa s a e excep ions wi h a
high equency o long ROH (> 30Mb, Fig.5) and FROH
alues o 0.14 and 0.15, espec i ely. The highly endan-
ge ed Mallo quina goa s ha e su e ed s ong popula ion
bo lenecks (cu en census = 150 indi iduals) [34]. The
Gi gen ana b eed has also expe ienced a s ong demo-
g aphic ecession om 30,000 indi iduals in 1983 o
461 in 1993 [37]. Thus, o bo h hese b eeds, long ROH
(> 30Mb) a e explained by popula ion bo lenecks and
ecen inb eeding.
As illus a ed by he Finnish, Danish and Du ch Lan-
d ace b eeds, gene ic isola ion may also occu in con i-
nen al popula ions ha a e aised in emo e loca ions
om Finland and Denma k o subjec o a s ic b eed-
ing managemen and selec ion in combina ion wi h he
occu ence o ounde e ec s (Ne he lands). The Du ch
goa popula ion has been e i ed since 1958: i s a ed
wi h wo emaining indi iduals, in ol ed undocumen ed
c ossb eeding and esul ed in he cu en popula ion o
ca. 2000 animals [14]. Gene ic dis ances show a ela ed-
ness o he Danish and Finnish Land ace popula ions,
which was no de ec ed by a panel o 26 mic osa elli es
[14]. Rema kably, he numbe s and leng h dis ibu-
ions o ROH o hese popula ions a e simila o hose
epo ed o B i ish ca le b eeds Angus, He e o d, Je sey
and Gue nsey [28], and la ge han hose epo ed o