Gene . Sel. E ol. 35 (2003) 533–557 533
© INRA, EDP Sciences, 2003
DOI: 10.1051/gse:2003038 O iginal a icle
Biodi e si y o 52 chicken popula ions
assessed by mic osa elli e yping
o DNA pools
Jossi H
ILLEL
a∗, Ma ien A.M. G
ROENEN
b,
Michèle T
IXIER
-B
OICHARD
c, Ab aham B. K
OROL
d, Lio D
AVID
a,
Vale y M. K
IRZHNER
d, Te y B
URKE
e, Asili B
ARRE
-D
IRIE
,
Richa d P.M.A. C
ROOIJMANS
b, Ka i E
LO
g, Ma cus W. F
ELDMAN
h,
Paul J. F
REIDLIN
a, Asko M
ÄKI
-T
ANILA
g, Ma ian O
ORTWIJN
b,
Pippa T
HOMSON
e, Alain V
IGNAL
i, Klaus W
IMMERS
j,
S e en W
EIGEND
aDepa men o Gene ics, The Heb ew Uni e si y o Je usalem,
Facul y o Ag icul u e, Food and En i onmen al quali y sciences,
Reho o 76100, Is ael
bIns i u e o Animal Sciences, Wageningen Ag icul u al Uni e si y,
Wageningen, The Ne he lands
cIns i u na ional de la eche che ag onomique, Cen e de Jouy-en-Josas, F ance
dIns i u e o E olu ion, Uni e si y o Hai a, Is ael
eDepa men o Animal and Plan Sciences, She ield Uni e si y, S10 2TN, UK
Ins i u e o Animal Science, Fede al Ag icul u al Resea ch Cen e,
Ma iensee, 31535 Neus ad , Ge many
gAg icul u al Resea ch Cen e, Ins i u e o Animal P oduc ion,
31600 Jokioinen, Finland
hDepa men o Biological Sciences, S an o d Uni e si y,
S an o d, CA 94305, USA
iIns i u na ional de la eche che ag onomique, Cen e de Toulouse, F ance
jIns i u e o Animal B eeding Science,
Rheinische F ied ich-Wilhelms-Uni e si a Bonn, Ge many
(Recei ed 2 Sep embe 2002; accep ed 13 Ma ch 2003)
∗Co espondence and ep in s
E-mail: [email p o ec ed]
534 J. Hillel e al.
Abs ac – In a p ojec on he biodi e si y o chickens unded by he Eu opean Commission
(EC), eigh labo a o ies collabo a ed o assess he gene ic a ia ion wi hin and be ween 52 pop-
ula ions om a wide ange o chicken ypes. Twen y- wo di-nucleo ide mic osa elli e ma ke s
we e used o geno ype DNA pools o 50 bi ds om each popula ion. The polymo phism meas-
u es o he a e age, he leas polymo phic popula ion (inb ed C line) and he mos polymo phic
popula ion (Gallus gallus spadiceus) we e, espec i ely, as ollows: numbe o alleles pe locus,
pe popula ion: 3.5, 1.3 and 5.2; a e age gene di e si y ac oss ma ke s: 0.47, 0.05 and 0.64; and
p opo ion o polymo phic ma ke s: 0.91, 0.25 and 1.0. These we e in good ag eemen wi h he
b eeding his o y o he popula ions. Fo ins ance, unselec ed popula ions we e ound o be mo e
polymo phic han selec ed b eeds such as laye s. Thus DNA pools a e e ec i e in he p elimina y
assessmen o gene ic a ia ion o popula ions and ma ke s. Mean gene ic dis ance indica es
he ex en o which a gi en popula ion sha es i s gene ic di e si y wi h ha o he whole es ed
gene pool and is a use ul c i e ion o conse a ion o di e si y. The dis ibu ion o popula ion-
speci ic (p i a e) alleles and he amoun o gene ic a ia ion sha ed among popula ions suppo s
he hypo hesis ha he ed jungle owl is he main p ogeni o o he domes ica ed chicken.
gene ic dis ance / polymo phism / ed jungle owl / DNA ma ke s / domes ica ed chicken
1. INTRODUCTION
I is widely accep ed ha all popula ions o domes ica ed chickens descend
om a single ances o , he Red Jungle Fowl (RJF) (Gallus gallus), o igina ing
in Sou heas Asia. Al hough i has been claimed ha o he wild species o
Gallus migh ha e con ibu ed o he domes ica ed chicken [5], he mo e widely
accep ed iew is ha Gallus gallus gallus alone is su icien o accoun o he
ma e nal ances y o he domes ica ed chicken [14,15]. A he p esen ime,
he imp o ed Medi e anean ype popula ions a e he mos closely ela ed
o he RJF, which we e he i s chickens b ough in o Eu ope [33]. Much
la e , wi h he massi e use o selec ion and c ossb eeding, local b eeds and
lines in di e en pa s o Eu ope we e de eloped, and Asian b eeds o he
Chinese and Malay ypes we e in oduced. All o hese sou ces con ibu ed
o he mode n biodi e si y o chicken popula ions. In e -c ossing, howe e ,
may ha e pa ly ex inguished di e ences among g oups o b eeds, wi h he
esul ha gene ic ela ionships be ween chicken popula ions a e no always
de ini i e. Fu he mo e, only some o hese sou ces we e used o de elop
he popula ions which cu en ly domina e he wo ld’s poul y indus y [6,27].
Since he s a o comme cial poul y b eeding in he middle o he 20 h cen u y,
chicken gene ic di e si y has become pa i ioned among ela i ely ew highly
specialized lines. As a consequence, many dual-pu pose b eeds, esul ing
om cen u ies o domes ica ion and b eeding, a e now a he isk o being los .
These b eeds may, howe e , ep esen a esou ce o genes o u u e b eeding
and esea ch pu poses. The e o e, i is necessa y o assess he di e si y a he
molecula le el in a wide ange o chicken popula ions, including comme cial
lines, adi ional b eeds, expe imen al lines and he ed jungle owl, in o de
o p o ide ecommenda ions ega ding u u e managemen o conse a ion o
Chicken biodi e si y assessed by DNA pools 535
hese popula ions. Al hough decisions on conse a ion o gene ic esou ce
popula ions should ely upon se e al sou ces o in o ma ion, including speci ic
ai s o in e es , molecula ma ke s may se e as an impo an ini ial guide [1].
In he p ocess o de eloping s a egies o conse e gene ic di e si y in domes ic
chickens, i is impo an o assess quan i a i ely he gene ic uniqueness o a
gi en popula ion [43], which may be deduced om gene ic dis ances.
Recen ad ances in molecula echnology ha e p o ided new oppo uni ies o
assess gene ic a iabili y a he DNA le el. Cu en ly, mic osa elli es a e widely
used since hey a e nume ous, andomly dis ibu ed in he genome, highly
polymo phic, and show co-dominan inhe i ance [20,30]. Many mic osa elli es
ha e ecen ly become a ailable in chickens, and ha e been mapped in e e ence
popula ions [4,8,9,22]. These ma ke s p o ide a powe ul ool o QTL
esea ch, and ha e also been success ully used o s udy he gene ic ela ionship
be ween and wi hin chicken popula ions [36,40,41,45,48]. Reliable in o m-
a ion on allele equencies was ob ained om chicken blood o DNA pools
using minisa elli e ma ke s [12,13,24,25], as well as mic osa elli es [10,31].
This a icle epo s on he esul s o he AVIANDIV EC- unded esea ch
p ojec [26,44,47]. The aim o he s udy was o e alua e he gene-pool o 52
chicken popula ions om a wide ange o o igins. The esul s may p o e o be
aluable o he u u e conse a ion o gene ic esou ces o chickens.
2. MATERIAL AND METHODS
Whe e possible and ele an , h oughou his epo , chicken lines, popula-
ions, and b eeds will be e e ed o as popula ions. Gene al in o ma ion on
hese popula ions is p esen ed in Table I and de ails we e epo ed by Tixie -
Boicha d e al. [44]. In o ma ion on he ma ke s is gi en in Table II and a b ie
desc ip ion o he popula ions, ma ke s and geno yping is gi en below.
2.1. Popula ions and animals
Fi y- wo popula ions we e chosen o ep esen as many Eu opean coun ies
as possible and o co e a wide ange o popula ions di e ing by selec ion
his o y and cu en managemen . We aimed o sample he same numbe
o males and emales om as many amilies as possible, o a o al o 50
chickens pe popula ion. Sampled popula ions we e classi ied a p io i in o
six ypes (Tab. I). Type 1 includes wo subspecies o he Red Jungle Fowl,
Gallus gallus gallus and G. g. spadiceus which we e ecen ly caugh in he wild.
Type 2 ep esen s i e domes ica ed bu unselec ed chicken popula ions wi h
subs an ial mo phological a ia ion. Type 3 ep esen s 23 s anda dized b eeds,
whe e selec ion has been done, ei he ecen ly o in he pas , on mo phological
ai s acco ding o a pheno ypic s anda d. Type 4 encompasses 13 expe imen al
o comme cial, whi e- o b own-egg laye lines. Type 5 includes eigh lines
536 J. Hillel e al.
Table I. In o ma ion on popula ions. (con inued on he nex page)
Popula ion Type
∗
O igin Founde
∗∗
C ea ion
∗∗∗
Size ( ange)
Name No.
Gallus gallus spadiceus 101 1 Thailand b 1997 100
Gallus gallus gallus 102 1 Thailand b 1997 165
Fayoumi 04 3 Egyp b 1978 50–300
Bedouin 05 2 Is ael a 1995 30–50
Wes aeliche To lege 06 3 Ge many b 1904 900
Sundheime 07 3 Ge many c 1886 100–500
Ligh B own Legho n 08 3 Ge many b 1870 (la ge)
Owl-bea ded (Uilenbaa de ) 09 3 The Ne he lands a 1650 200
F iesian owl 10 3 The Ne he lands a (unknown) 50
B esse noi e 11 4.2 F ance b 1995 400–2500
Houdan 12 3 F ance c 1994 50–200
Ma ans 13 3 F ance c 1988 200–350
Do king 14 3 G ea -B i ain b 1986 85
Cochin 15 3 China b 1946 130
Icelandic land ace 16 2 Iceland a 900 2000–4000
Finnish Land ace 17 2 Finland c 1900 600–1000
Old Scand. Re . Pop. 18 3 Denma k c 1969 200–700
Jae hoens 19 3 No way a 1916 300–400
Sicilienne Bu e cup 20 3 I aly- Sicilia b 1990 150
Pado ana 21 3 I aly b 1986 35–350
Black Cas ellana 22 3 Spain a 1975 200–300
Red Villa anquina 23 3 Spain a 1980 200–300
Czech Golden Pencilled 24 3 Czech Republic c 1995 500–1000
O a ka hen 25 3 Slo akia c 1994 50–100
T anssyl . Naked Neck 26 3 Hunga y a 1990 70–220
G een-legged Pa idge 27 3 Poland a 1950 1600
O lo 28 3 Russia c 1960 2000
Yu lo c owe , in Russia 2901 3 Russia c 1976 10 000
Yu lo c owe , in Uk ainia 2902 2 Uk aine b 1870 140–700
Uk ainian bea ded 30 2 Uk aine b 1850 74–105
Pol a a clay 31 3 Uk aine b 1870 2000–6000
C line 32 6 Czech Republic a 1932 180–600
Gödöllö Nhx, 33 4.15 Hunga y c 1996 600–8000
Line Sa coma-Resis an 3401 4.10 USA, now in
Ge many
b 1965 200
Line Sa coma-Suscep ible 3402 4.10 USA, now in
Ge many
b 1965 200
Whi e-egg laye A 37 4.3 comme cial b 1959 6000
B own-egg laye A 38 4.4 comme cial b 1979 5000
B oile dam line A 39 5.1 comme cial c 1980 10 000
B oile si e line A 40 5.2 comme cial c 1980 10 000
B oile dam line B 41 5.1 comme cial a 1960 5000–30 000
B oile si e line B 42 5.2 comme cial b 1970 10 000–70 000
B own-egg laye B 43 4.4 comme cial c 1960 5000
B own-egg laye line C 44 4.4 comme cial b 1960 5000
B own-egg laye line D 45 4.4 comme cial b 1962 1000
Chicken biodi e si y assessed by DNA pools 537
Table I. Con inued.
Popula ion Type
∗
O igin Founde
∗∗
C ea ion
∗∗∗
Size ( ange)
Name No.
B own-egg laye line E 46 4.4 comme cial b 1955 600
B oile si e line C 47 5.2 comme cial a 1974 con iden iel
B oile dam line C 48 5.1 comme cial a 1974 con iden iel
B oile si e line D 49 5.2 comme cial a 1992 8000
B oile dam line D 50 5.1 comme cial b 1970 5000–20 000
Ab line, high 51 4.15 The Ne he lands c 1980 75–300
Ab line, low 52 4.15 The Ne he lands c 1980 75–300
Ab line, con ol 53 4.15 The Ne he lands c 1980 110–250
∗ ype: 1 =wild popula ion; 2 =domes ica ed unselec ed b eed; 3 =s anda dized b eed selec ed
on mo phology; 4 =Laye s, selec ed on quan i a i e ai s; 5 =B oile s, selec ed on quan i a i e
ai s; 6 =inb ed line.
De ailed in o ma ion o ype 4: 4.10 =expe imen al Whi e Legho n; 4.15 =expe imen al
b own egg laye ; 4.2 =comme cial whi e egg laye no Whi e Legho n; 4.3 =comme cial Whi e
Legho n; 4.4 =comme cial b own-egg laye .
De ailed in o ma ion o ype 5: 5.1 =comme cial b oile dam line; 5.2 =comme cial b oile
si e line.
∗∗ ounde : a =small lock; b =one b eed; c =a c oss be ween se e al b eeds.
∗∗∗ es ima e o he C ea ion Time o he sampled locks.
o mea ype chickens: ou b oile dam-lines and ou b oile si e-lines. Fo
lines o ypes 4 and 5, selec ion has been applied on a quan i a i e ai o on
an index. Expe imen al lines included wo se s o di e gen ly selec ed lines.
Type 6 is an inb ed line.
2.2. Blood and DNA samples
Blood samples o 2–4 mL we e collec ed om he wing ein wi h Sa s ed
Sy inges con aining EDTA as an an i-coagula ing agen . In 20 popula ions,
blood samples we e collec ed on he same day and blood cells om indi idual
bi ds we e ob ained om esh blood by cen i uga ion and we e e-suspended
in an equal olume o PBS/Suc ose (1 /1 ). DNA pools om each popula ion
we e used o educe he amoun o geno yping. An aliquo o 50 µL o blood
cells in PBS/Suc ose om each bi d in a popula ion was aken o p epa e i s
blood pool. Indi idual blood samples and blood pools we e ozen a −25 ◦C.
High molecula weigh DNA was ex ac ed om 80 µL o he blood pool,
ollowing se e al s eps o haemolysis, p o einase K incuba ion, p ecipi a ion
in dime hyl- o mamide/ace one (95 /5 ), e-suspension in TE, e hanol p ecip-
i a ion and inal e-suspension in 2 mL TE. Fo he o he 32 popula ions, a blood
pool could no be made p ope ly, ei he because he indi idual blood samples
had been ozen, o because hei quali y was no good enough. Consequen ly,
DNA was ex ac ed om indi idual blood samples and he pooled DNA sample

538 J. Hillel e al.
Table II. Polymo phism measu es o he 22 mic osa elli es; ma ke names, loca ion: ch omosome and posi ion, allele size ange,
numbe o alleles ac oss popula ions and pe popula ion, a e age, minimum and maximum alues o gene di e si y and equency o
polymo phic popula ions. Loci a e so ed by dec easing a e age alues o gene di e si y.
Ma ke Loca ion Allele size* Numbe o alleles Gene di e si y F eq. polym.
popula ions (P)
Ch omosome Posi ion A e . S.D. Range
(bp)
Ac oss
popula ions
Pe
popula ion
A e . Min. Max.
MCW34 2 230 230 5.9 30 16 6.5 0.68 0.19 0.88 0.98
ADL268 1 288 112 3.3 20 10 4.5 0.63 0.13 0.78 0.98
MCW69 E60C04W23 23 161 4.1 23 12 5.4 0.61 0.18 0.88 1.00
LEI192 6 114 271 14.7 74 23 5.4 0.59 0.28 0.80 0.96
MCW183 7 79 307 8.2 36 16 5.1 0.59 0.02 0.81 0.92
ADL112 10 0 132 2.5 12 7 3.8 0.55 0.15 0.75 1.00
MCW295 4 75 96 3.6 16 9 3.4 0.51 0.15 0.80 0.94
MCW206 2 104 233 4.1 31 14 4.0 0.51 0.07 0.77 0.98
MCW111 1 118 104 2.3 20 9 3.6 0.51 0.13 0.75 1.00
MCW14 6 96 184 5.7 26 13 4.2 0.50 0.11 0.78 1.00
MCW330 17 41 280 8.9 39 10 3.1 0.48 0.10 0.81 0.86
ADL278 8 87 118 4.2 15 5 2.8 0.47 0.32 0.71 0.92
MCW78 8 87 143 2.5 13 7 3.4 0.44 0.16 0.73 0.90
MCW37 3 317 157 1.5 8 5 2.4 0.43 0.03 0.67 0.87
MCW67 10 61 181 2.8 10 6 2.5 0.41 0.06 0.74 0.92
MCW81 5 123 122 8.7 23 12 4.2 0.41 0.02 0.79 0.88
MCW222 3 86 223 2.1 10 6 2.4 0.39 0.02 0.71 0.85
MCW216 13 28 146 1.4 14 6 2.2 0.38 0.06 0.67 0.86
MCW284 4 167 245 4.8 46 10 2.0 0.33 0.13 0.81 0.84
MCW103 3 210 273 2.0 12 7 2.5 0.33 0.10 0.66 0.86
MCW248 1 20 218 2.7 10 5 2.1 0.31 0.04 0.66 0.71
MCW98 4 217 264 1.0 6 4 1.8 0.29 0.06 0.55 0.69
A e age 191 4.4 22.4 9.6 3.5 0.47 0.11 0.75 0.91
∗allele size =size o he PCR p oduc which includes he mic osa elli e epea s.
Chicken biodi e si y assessed by DNA pools 539
was p epa ed by aliquo ing equal amoun s o indi idual DNA, as measu ed by
spec opho ome y. P io o geno yping, he concen a ion o he DNA pools
was s anda dized o 100 ng ·µL−1in TE solu ion. The geno yping o he 52
popula ions was done o 22 mic osa elli e loci.
2.3. Geno yping a mic osa elli e loci
A se o 22 (CA)n di-nucleo ide mic osa elli e ma ke s, which a e as uni-
o mly dis ibu ed as possible h oughou he chicken genome, was es ed
o hei use in DNA pools. The ma ke s and hei genomic posi ion a e
lis ed in Table II. Peak sco ing on an ABI sequence was used o es ima e
mic osa elli e allele equencies as de ailed in C ooijmans e al. [10]. PCR
p oduc s o di e en ma ke s we e pooled in such a way ha each ma ke
signal on he ABI sequence s did no exceed a peak heigh o abou 1000
o 1500. F agmen sizes we e de e mined ela i e o he GENESCAN-350
TAMRA wi h he GENESCAN agmen analysis so wa e (Pe kin Elme ,
Applied Biosys ems Di ision). Subsequen ly GENOTYPER so wa e (Pe kin
Elme , Applied Biosys ems Di ision) was used o au oma ed agmen calling
and he gene a ion o an ou pu able con aining he agmen s o he di e en
loci and he peak a eas o each o hese agmen s. Finally, hese peak a eas
we e used o calcula e he ela i e agmen equencies o all peaks o each
locus. These equencies we e used in his s udy as he allele equencies.
Howe e , alleles sco ed om DNA pools using an ABI sequence , migh
be a e ac s and s u e bands a he han eal alleles. We assumed ha his
di icul y would be ele an equally o all popula ions and mos ma ke s.
2.4. Gene di e si y es ima e
Using he calcula ed allele equencies Pmi o popula ion mand allele i, gene
di e si y (Hm), namely he expec ed he e ozygosi y unde Ha dy-Weinbe g
assump ions, is:
Hm=1−X
i
P2
mi.(1)
An a e age Hwas calcula ed o each locus ac oss popula ions and o each
popula ion ac oss loci.
2.5. Gene ic dis ance es ima es
Th ee gene ic dis ances based on allele equencies we e used: he Nei
gene ic dis ance [34], Ca alli-S o za cho d measu e [3] and Reynolds gene ic
dis ance [38]. Addi ionally, he del a-mu-squa ed dis ance [18,19], based
on allele size, was applied. Pai wise dis ances be ween each pai o he 52
popula ions (1326 es ima es) we e calcula ed o each measu e.
540 J. Hillel e al.
2.6. S a is ical analyses
Co ela ion coe icien s and ank co ela ions we e es ima ed using JMP 4.0
so wa e [28].
2.7. Calcula ion o he mu a ion a e
We used he in o ma ion on he his o y o he wo Sa coma lines 3401 and
3402 (see Tab. I) and hei mic osa elli es da a o es ima e he mu a ion a e o
mic osa elli es in chickens. These lines we e di e gen ly selec ed o esis ance
o suscep ibili y o Rous Sa coma Vi uses (RSV) A and B o 2- o-3 wk old
chickens [23]. The wo sub-lines ha e been kep sepa a ely o 25 gene a ions.
The wo lines had 74 di e en alleles o which only 46 (62%) we e sha ed. A
each o he 25 gene a ions, en si es we e selec ed om each line and ma ed o
app oxima ely 100 dams. In his p ocess, 220 game es we e in ol ed a each
gene a ion and o each line, o p oduce he nex gene a ion. We sco ed he
numbe o mic osa elli e alleles speci ic o each o he wo lines in compa ison
o he o he one.
3. RESULTS
Raw da a and basic esul s such as gene ic dis ances be ween popula ion pai s
o he cu en s udy, can be ob ained om he Poul y Biodi e si y da abase a :
h p://w3. z . al.de/a iandi /index.h ml.
A o al o 3760 allele equencies we e ob ained. Amongs he 1144 possible
ypings (22 ma ke s ×52 popula ions), 77 (6.7%) we e missing due o echnical
di icul ies, mainly o h ee loci: ADL278,MCW14, and MCW330, wi h
missing da a on 27, 15, and 15 popula ions, espec i ely. Fo he emaining 19
ma ke s, only 20 (2.0%) geno yping da a poin s we e missing.
3.1. Polymo phism o ma ke s
As shown in Table II, all 22 ma ke s we e polymo phic in a leas 69% o he
popula ions, and 91% o he popula ions we e polymo phic. The mean numbe
o alleles was 9.6 ac oss popula ions and 3.5 wi hin popula ions, and a e age
gene di e si y was 0.47. Among he 22 es ed ma ke s, he mos polymo phic
was MCW34 wi h 16 alleles ac oss popula ions and, on a e age, 6.5 alleles pe
popula ion. The gene di e si y o MCW34 was 0.68 and 98% o he popula ions
we e polymo phic o his ma ke . A he o he ex eme, ma ke MCW98 was
he leas polymo phic, wi h ou alleles ac oss popula ions, 1.8 alleles pe
popula ion, and a gene di e si y o 0.29; in addi ion i was polymo phic in 69%
o he popula ions.
Chicken biodi e si y assessed by DNA pools 541
Table III. Co ela ion coe icien s be ween polymo phism measu es o ma ke s and
hei s a is ical signi icance (p).
Polymo phism measu e Alleles ac oss
popula ions
Alleles pe
popula ion
Expec ed
he e ozygosi y
Size di e ence 0.87 0.51 0.41
(0.00001) (0.01) (n.s.†)
Alleles ac oss popula ions 0.81 0.65
(<0.00001) (0.0011)
Alleles pe popula ion 0.91
(<0.00001)
†n.s. =non signi ican .
The associa ions be ween he a ious measu emen s o ma ke polymo ph-
ism a e p esen ed in Table III. The numbe o alleles ac oss he popula ions
was highly co ela ed wi h he di e ence be ween he smalles and he la ges
allele a a locus ( =0.87) and as expec ed, wi h he numbe o alleles pe
popula ion ( =0.81). Gene di e si y was highly co ela ed wi h he numbe
o alleles pe popula ion ( =0.91) bu o a lesse ex en wi h he numbe o
alleles ac oss popula ions ( =0.65). Based on hese associa ions, i u ned
ou ha he ma ke s LEI192 and MCW284 had mo e alleles ac oss popula ions
han expec ed om hei a e age numbe o alleles pe popula ion and ma ke
MCW34 had less alleles ac oss popula ions han expec ed om i s a e age pe
popula ion.
3.2. Di e si y o popula ions
Table IV p esen s he di e si y measu es o he 52 popula ions. A e age
gene di e si y (H) wi hin he 52 popula ions ac oss all 22 loci was 0.47 and he
a e age numbe o alleles was 3.5. The leas polymo phic popula ion was he
inb ed “C line”, wi h a gene di e si y (H) o 0.05 and 1.3 alleles pe locus ac oss
all ma ke s. The nex o lowes was Pado ana, a ancy b eed wi h a na ow
base in No he n I aly, wi h H=0.17, and 1.8 alleles. The mos polymo phic
popula ion was he Gallus gallus spadiceus, wi h H=0.64 and an a e age
o 5.2 alleles, ollowed by he popula ion o Yu lo C owe in Russia, wi h
H=0.62 and 4.8 alleles.
Wi hin hese ex eme popula ions, he e was a ia ion ac oss ma ke loci.
In he inb ed C line, he polymo phism anged om H=0.39 and wo alleles
o ma ke ADL268 o H=0 a 15 o he emaining loci. Simila ly, in Gallus
gallus spadiceus, polymo phism a ied be ween H=0.88 and 11 alleles
(MCW69), o H=0.20 and 2 alleles (MCW222).
548 J. Hillel e al.
4. DISCUSSION
4.1. Da a eliabili y
In gene al, he esul s epo ed he e we e in good ag eemen wi h wha is
known o he his o y o he popula ions and wi h p e ious scien i ic epo s.
Fo ins ance, he e al popula ions and he domes ica ed unselec ed popula ions
we e he mos polymo phic, while he inb ed and he Whi e Legho n lines we e
a less polymo phic. This sugges s ha use o DNA pools, he chosen ma ke s
and he biome ical ools desc ibed in his epo , p o ide eliable es ima es
o he popula ion’s biodi e si y (see also [10,12,13,24,25,31]). Fu he mo e,
polymo phism es ima es ob ained om hese DNA pools we e ound o be in
good ag eemen wi h hose ob ained om indi idually yping a subse o 30
bi ds om 20 popula ions (unpublished da a). Fo ins ance, he co ela ion
coe icien be ween H alues o he cu en s udy and obse ed he e ozygo e
equency is =0.85 (p=0.002)and be ween he numbe o alleles pe
locus is =0.91 (p=0.0002). Da a eliabili y was also suppo ed by he
same o de o popula ion H alues, based on 22 subse s, wi h single ma ke s
sys ema ically excluded.
4.2. Di e si y o mic osa elli es and i s mu a ion a e
The wide ange o biodi e si y in he sampled popula ions and he high le el
o polymo phism o mic osa elli es we e e lec ed by he inding ha e en
he leas polymo phic locus, MCW98 was ound o be polymo phic in 69%
o he popula ions while ou o he 22 ma ke s we e polymo phic in all 52
popula ions (Tab. II).
The co ela ion coe icien s be ween some o he polymo phism measu es
a e high and e y signi ican ( =0.81 −0.91, see he diagonal o Tab. III).
On he con a y, allele-size ange had lowe co ela ion coe icien s wi h he
numbe o alleles pe popula ion (na)( =0.51, p<0.01) and wi h he
expec ed he e ozygo e equency H( =0.41, p>0.05). On close exam-
ina ion, o h ee loci, namely LEI92,MCW284 and MCW330, size anges
a e la ge han expec ed, based on hei naand H alues. Fo LEI192, six o
he six een alleles ac oss popula ions we e p esen in only a single popula ion
and wo alleles in wo popula ions. Excluding hese eigh alleles, educed
he ange om 74 bp o 46 bp. Simila ea men o he loci MCW284 and
MCW330 educed he numbe o alleles ac oss popula ions om ele en o wo
and om en o ou , espec i ely. Simila ly, allele size anges educed om
46 bp o 8 bp o MCW284 and om 39 bp o 30 o MCW330. These can
be in e p e ed ei he as popula ion-speci ic (p i a e) alleles o as signal peaks
in he sequence machine ha a e no alleles. Disc imina ion be ween hese is

Chicken biodi e si y assessed by DNA pools 549
possible only by analyzing sibships, which is ou o he scope o he p esen
epo .
In s udies o human gene ic a ia ion, a he con inen al le el he e is good
ag eemen in he o de ing by egion o gene di e si y measu es among di e en
kinds o ma ke s, once asce ainmen bias is emo ed [29,39]. The same
is ue o he o de ing o gene ic dis ances among popula ions assessed o
di e en ma ke s [29]. I is easonable he e o e o belie e, ha he o de ing
among chicken b eeds o di e si y and dis ances seen he e o mic osa elli es
in DNA pools would no be e y di e en o o he gene ic ma ke sys ems.
The mic osa elli e loci used he e we e selec ed o be polymo phic o use in
gene mapping. Howe e , Rosenbe g e al. [42] ob ained di e si y and gene ic
dis ance pa e ns o humans ha la gely ag eed wi h hose o Bowcock e al. [2]
e en hough he o me s udy used mic osa elli es om a mapping se and he
la e used ma ke s ha we e no selec ed. Asce ainmen bias is, he e o e, no
expec ed o ha e had a majo e ec on he o de ing o s a is ics o ou chicken
da a.
The es ima ion o he mu a ion a e using he di e gen ly selec ed (RSV)
lines is based on he assump ion ha he 22 mic osa elli e ma ke s a e no
linked o genes ha a e a ec ed by he selec ion c i e ia. Webe and Wong
ound a mu a ion a e o 5.6×10−4 o di-nucleo ide loci in humans by pedig ee
analysis [46]. Based on 22 di-nucleo ide loci, ou es ima e was abou i e imes
lowe , bu may unde es ima e he ac ual alue since i was assumed ha no
e e se o ecu en mu a ions occu ed. Since his es ima e is om a single
se o di e gen ly selec ed lines, we canno es ima e con idence limi s o his
a e. Fu he analysis o chickens is needed o p o ide a eliable es ima e o
mu a ion a e.
4.3. Gene ic di e si y o popula ions
A gene di e si y o 0.48 was ob ained om DNA pools in a subse o 20
popula ions. Based on indi idual yping o he same subse , he equency o
he e ozygo es was 0.47 (unpublished da a). These es ima es a e simila o he
a e age Hin all 52 popula ions indica ing he good eliabili y o ou es ima es.
Di e si y es ima es in his s udy a e lowe han he obse ed equencies o
he e ozygo es epo ed in o he species using mic osa elli e ma ke s. Fo
ins ance, in human popula ions he a e age he e ozygo e equency anges
be ween 0.7 and 0.8 [2], in ca le- 0.6 [11], in pigs- 0.68 [21] and in ish-
0.86 [16]. Al hough such compa isons a e di icul o in e p e , he lowe
a iabili y in chickens calls a en ion o he impo ance o conse ing he
chicken gene pool. I is wo h men ioning, howe e , ha SNP equency
in he chicken genome was ound o be qui e high and signi ican ly highe han
ha ound in he human genome (unpublished da a).
550 J. Hillel e al.
4.4. Di e si y be ween popula ions wi hin ypes
Ca ego iza ion o popula ions in his s udy was done acco ding o he pop-
ula ions’ his o y and hei b eeding pu pose, which ha e a ec ed he gene ic
di e si y. Indigenous s ocks a e domes ica ed bu unselec ed local b eeds
( ype 2) ha ha e pe sis ed in he ag icul u al socie ies o decades o e en
cen u ies. Thei long his o y in ce ain egions migh ha e led o speci ic
adap a ion o local en i onmen al condi ions and gene ic changes due o na u al
selec ion and o some deg ee due o gene ic d i as well. In p ac ice, ou ou
o he i e popula ions o ype 2 had ela i ely high polymo phism, which may
e lec hei a he la ge e ec i e popula ion size and he ac ha hese s ocks
we e no subjec ed o in ense selec ion o p oduc ion.
The g oup o s anda dized b eeds ( ype 3) selec ed o mo phological ai s
co e s a wide ange o a ious b eeds kep by ancie s. This ype has la ge
a iance in polymo phism le els (Tab. IV) as also e lec ed in he sca e ed
pa e n o i s popula ions in Figu e 1. Based on gene ically dis inc local popu-
la ions, pu e b eeds we e de eloped ha di e ed in many pheno ypic ai s such
as plumage colo , plumage pa e n, and comb ype. Gene ic changes in ancy
b eeds may occu a he apidly in hese ela i ely small popula ions because o
in ense selec ion o exhibi ion ai s, inb eeding, c ossb eeding gene ic d i ,
bo leneck and ounde e ec s [17,35,36]. This complexi y o his o ies and
b eeding p ac ices may explain he he e ogenei y o polymo phism alues ha
cha ac e izes ype 3.
Types 4 (laye s) and 5 (b oile s) o chicken lines, which a e selec ed o
quan i a i e ai s, encompass he majo comme cial poul y indus y. Es im-
a es o b oile s (H=0.57) we e in ag eemen wi h a p e ious epo , in which
H=0.53 was ob ained om pooled blood samples [10]. The Whi e Legho n
laye line in ou s udy (sub- ype 4.3) was ound o ha e low gene di e si y
(0.33), sligh ly highe han he alue o 0.27 in he p e ious epo [10]. Among
he laye s his line had he lowes polymo phism.
In he 1940s, poul y b eeding began o de elop as a business. Pu e b ed
lines we e used o de elop specialized comme cial b eeding s ocks o able
egg and mea p oduc ion by applying highly e icien and in ense b eeding
p og ams. Indus ial egg and mea s ocks a e b ed by la ge mul ina ional
b eeding companies, and he “end p oduc s” a e hyb ids based mos ly on ou
highly selec ed g andpa en al lines. In pa icula du ing he las decades e o s
ha e been made o limi inb eeding in hese g andpa en al pu e b ed lines [37].
La ge lock sizes and limi ing inb eeding may be e lec ed by he deg ee o
polymo phism o hese ypes (4 and 5) which is compa able e en o hose
o popula ions ha we e no subjec ed o in ensi e b eeding. I should be
no ed he e ha he comme cial lines in ou s udy a e all pu e b ed lines.
The e o e, hei le el o polymo phism can be conside ed as a eliable es ima e
o he polymo phism o he pu e-b ed g andpa en al lines. Di e ences wi hin
Chicken biodi e si y assessed by DNA pools 551
ypes 4 and 5 migh be explained by he di e en o igin o whi e egg laye s,
b own egg laye s and b oile s. Whi e egg laye s a e chie ly ep esen ed by
one b eed, he Single Comb Whi e Legho n b eed, while he gene ic basis
o b own egg laye s has been somewha b oade , mainly coming om he
Rhode Island Red, New Hampshi e, Plymou h Rock and Aus alo p b eeds.
A simila pic u e is cha ac e is ic o he poul y mea p oduc ion sec o . The
pa e nal g andpa en lines a e mainly de i ed om he Whi e Co nish b eed,
while ma e nal g andpa en s a e hea ily based on Whi e Plymou h Rocks. The
Co nish was de eloped in England om Asia ic igh ing s ocks, and he Whi e
Plymou h Rock was de i ed om an Ame ican pa en b eed [6].
The low deg ee o gene di e si y in he inb ed C line esul ed di ec ly om
he b o he -sis e ma ing scheme used o de elop his line and possibly om
gene ic d i due o he limi ed e ec i e popula ion size.
4.5. Gene ic dis ance measu es
The h ee gene ic dis ance measu es which a e based on gene equencies
we e in good ag eemen wi h he gene ic di e si y o he examined b eeds,
indica ing ha hese app oaches i he his o y o he domes ica ed chickens
well. Howe e , he (δµ)2app oach ha is based on he allele size which
is ypical o mic osa elli es, was di e en and poo ly co ela ed wi h o he
gene ic dis ances as well as measu es o di e si y. P obably he his o y o
he domes ica ed chicken does no mee he assump ions behind his app oach
especially he cons an popula ion size.
4.6. Concep ual aspec s o MGD
A domes ica ed popula ion wi h a la ge numbe o alleles pe locus is
expec ed o ep esen a la ge po ion o he s udied gene pool and he e o e
o be gene ically close o all o he popula ions. Popula ions o ypes 1 and 2
a e polymo phic and ep esen he gene pool well and indeed ha e low alues
o MGD. On he con a y, popula ions ha a e ela i ely monomo phic canno
e lec he whole s udied gene pool and he e o e will ha e high MGD alues,
as e idenced by he inb ed C line and a ew popula ions om ypes 3 and 4.3.
Figu e 1 shows a nega i e and clea associa ion be ween he a e age numbe
o alleles pe locus and he Ca alli-S o za MGD alues. A simila and igh e
associa ion is appa en when gene di e si y alues a e examined. The clea
associa ion discussed abo e be ween polymo phism and MGD alues sugges s
ha he app oach o cons uc ing e olu iona y ees in domes ica ed popula ions
is likely o gi e a misleading pic u e o he his o y. This is pa icula ly ue
o oo ed ees, which assume a unidi ec ional e olu iona y p ocess. I seems
ha he p ocesses o domes ica ion and b eeding ha e in ol ed mo e o less
con inuous and mul idi ec ional gene low.
552 J. Hillel e al.
Ca e ul examina ion o Figu e 1 e eals ha popula ions wi h a simila
numbe o alleles may ha e di e en MGD alues. The join dis ibu ion o
he numbe o alleles and MGD alues can be iewed wi h a eg ession line
ha will be e med a “ end line”, as in Figu e 1. The unselec ed popula ions
( ype 2) a e highly polymo phic and loca ed nex o o below he end line,
implying ha many o hei alleles a e common o he s udied gene pool. The
wo Gallus gallus subspecies ha e a la ge numbe o alleles pe locus bu a e
bo h loca ed abo e he end line, which implies some p opo ion o p i a e
alleles. Indeed, i e p i a e alleles ha a e absen in he domes ica ed chicken
we e ound o be p esen in G. g. gallus and six such alleles in G. g. spadiceus.
4.7. The chicken ances o and he need o conse a ion
I is assumed ha all b eeds o he domes ica ed chicken descend om a
single ances o , he RJF, which o igina ed in Sou heas Asia [5,14,15]. Since
popula ions a he cen e o o igin should con ain he highes di e si y (as has
been shown o humans and o he species [2]), RJF should p esen a high le el
o polymo phism and also hold low alues o MGD. The wo sub-species o
Gallus gallus (RJF) which a e ep esen ed in his s udy ha e high di e si y
alues and low MGD alues, bu no he lowes (Tab. IV and Fig. 1). These
esul s sugges he hypo hesis ha he Red Jungle Fowl is a majo con ibu o o
he gene pool o he domes ica ed chicken. The p esence o p i a e alleles bo h
in he RJF and in he domes ica ed gene pool does no necessa ily con adic his
hypo hesis. These p i a e alleles could esul om gene ic d i and sepa a e
e olu ion since he onse o domes ica ion. Addi ionally, p i a e alleles o
he domes ica ed b eeds may indica e a con ibu ion o o he wild species as
deba ed in C aw o d [5]. In s udies on he mi ochond ial DNA in chickens [14,
15], he au ho s sugges ha Gallus gallus gallus could ha e gi en ise o he
di e se b eeds o he domes ica ed chicken, e en hough common pa e ns in
domes ica ed b eeds and in G. g. spadiceus and G. g. banki a a e also obse ed.
Wi h ega ds o he le el o gene ic polymo phism and he mean gene ic
dis ance, he Red Jungle Fowl (Gallus gallus) appea s o be an impo an
ese oi o he chicken polymo phism. Ne e heless, du ing domes ica ion,
ex ensi e gene ic di e si y has accumula ed in he chicken, and his di e si y is
displayed by he many b eeds and s ains di e ing in hei pheno ypes which
a e he p oduc s o many gene ic, en i onmen al and managemen egimes.
A comple e desc ip ion o each b eed o popula ion would en ail asce aining
all genes ha con ibu e o any pheno ypic ai . I is e y unlikely ha such
comple e knowledge can be achie ed in he nea u u e. The e o e, a mo e
p ac ical al e na i e is needed. We belie e ha in o ma ion om DNA ma ke s
oge he wi h pheno ypic pe o mance and popula ion his o y may p o ide
eliable guidelines in choosing popula ions o p ac ical and o conse a ion
pu poses. Howe e , se ing conse a ion p io i ies based exclusi ely on he
Chicken biodi e si y assessed by DNA pools 553
di e si y o molecula ma ke s migh lead o he loss o locally adap ed
popula ions [32].
In ecen yea s, b eede s o comme cial whi e-egg laye s ha e been con-
ce ned abou educed gene ic a iabili y and u u e esponse o selec ion. The
esul s epo ed in he p esen a icle suppo his conce n, pa icula ly o
Whi e Legho n b eeds. The massi e me ging o b eeding companies in ecen
yea s should call o a en ion o he need o conse a ion o gene ic a ia ion
among b eeds and lines. App op ia e s a egies o conse a ion o popula ions
is ou o he scope o he p esen epo bu is an impo an and con o e sial
issue [7]. Ou esul s emphasize he need o conse e polymo phic popula ions
such as Yu lo C owe , he O lo o he Finnish Land ace o he sake o
global a iabili y, and o p ese e small popula ions o hei unique gene ic
ea u es. MGD alues can assis in choosing popula ions mos aluable o he
p ese a ion o gene ic a ia ion.
ACKNOWLEDGEMENTS
We wish o hank Jean-Luc Co ille and Camilo Vilela-Lamego, In a, Jouy-
en-Josas, F ance, who we e in ol ed in he DNA p epa a ion and i s dis i-
bu ion, and o he ollowing sub-con ac o s who p o ided he blood samples
and b eed desc ip ions; wi hou hei help his s udy could no ha e been
pe o med ( hey a e lis ed alphabe ically): D . G. Baldane, Pado a, I aly; D .
J. Baumga ne , Resea ch Ins i u e, I anka p i Dunaji, Slo akia; D . Y. Bond-
a enko, Resea ch Ins i u e; Bo ky, Kha ki , Alaska; D . J.L. Campo, INIA,
Mad id, Spain; D. Cassu o, ANAK, Is ael; D . K. Cywa-Benko, Resea ch
Ins i u e, Balice n C acow, Poland; D . E. Ey ho sdo i , RALA, Is ael; Y.
Jego, Hubba d-ISA, F ance; D . J. Ka hle, NLH, No way; D . I. Moiseye a,
Resea ch Ins i u e, Gubkin, Moscow, Russia; D . G. Pidone, Cala a imi, I aly;
P o . R. P eisinge Lohmann, Ge many; M. P o ais, Hubba d-ISA, F ance; P.
Raul , SYSAAF, Tou s, F ance; M s. V. Robe s, UK; D . P. So ensen, DIAS,
Denma k; D . I. Szalay, Hunga y; P o . The dchai Vea asilp, Thailand; D .
B. Tho p Ross B eede s, A iagene, UK; D . P. T e il, Biopha macy Ins i u e,
P ague, Czech Republic; F. an Sambeek, Hend ix, Ospel, The Ne he lands;
D .Vilhelmo a, Czech Republic; J. Vincen , Cobb, UK; D . G. Vi ag, Resea ch
Ins i u e, Godollo, Hunga y.
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