Dual origins of dairy cattle farming - evidence from a comprehensive survey of European Y-chromosomal variation

Dual O igins o Dai y Ca le Fa ming – E idence om a Comp ehensi e Su ey o Eu opean Y-Ch omosomal Va ia ion Cei idwen J. Edwa ds 1,2 , Ca a ina Ginja 3,4 , Juha Kan anen 5 ,Lucı ´aPe ´ ez-Pa dal 6 , Anne T esse 7 , F auke S ock 1 , Eu opean Ca le Gene ic Di e si y Conso ium " , Luis T. Gama 4 , M. Cecilia T. Penedo 3 , Daniel G. B adley 1 , Johannes A. Lens a 8 *, Isaa ¨c J. Nijman 8¤ 1Smu i Ins i u e o Gene ics, T ini y College Dublin, Dublin, I eland, 2Resea ch Labo a o y o A chaeology, Uni e si y o Ox o d, Ox o d, Uni ed Kingdom, 3Ve e ina y Gene ics Labo a o y, Uni e si y o Cali o nia Da is, Da is, Cali o nia, Uni ed S a es o Ame ica, 4Depa amen o de Gene ´ ica, Melho amen o Animal e Rep oduc¸a ˜o, Ins i u o Nacional dos Recu sos Biolo ´gicos, Fon e Boa, Vale de San a e ´m, Po ugal, 5Bio echnology and Food Resea ch, MTT Ag i ood Resea ch Finland, Jokioinen, Finland, 6A ea de Gene ´ ica y Rep oduccio ´n Animal, SERIDA, Gijo ´n, Spain, 7A che ´ozoologie, A che ´obo anique, Socie ´ e ´s, P a iques e En i onnemen s, CNRS Muse ´um Na ional d’His oi e Na u elle, Pa is, F ance, 8Facul y o Ve e ina y Medicine, U ech Uni e si y, U ech , The Ne he lands Abs ac Backg ound: Di e si y pa e ns o li es ock species a e in o ma i e o he his o y o ag icul u e and indica e uniqueness o b eeds as ele an o conse a ion. So a , mos s udies on ca le ha e ocused on mi ochond ial and au osomal DNA a ia ion. P e ious s udies o Y-ch omosomal a ia ion, wi h limi ed b eed panels, iden i ied wo Bos au us ( au ine) haplog oups (Y1 and Y2; bo h composed o se e al haplo ypes) and one Bos indicus (indicine/zebu) haplog oup (Y3), as well as a s ong phylogeog aphic s uc u ing o pa e nal lineages. Me hodology and P incipal Findings: Haplog oup da a we e collec ed o 2087 animals om 138 b eeds. Fo 111 b eeds, hese we e esol ed u he by geno yping mic osa elli es INRA189 (10 alleles) and BM861 (2 alleles). Eu opean ca le ca y exclusi ely au ine haplo ypes, wi h he zebu Y-ch omosomes ha ing app eciable equencies in Sou hwes Asian popula ions. Y1 is p edominan in no he n and no h-wes e n Eu ope, bu is also obse ed in se e al Ibe ian b eeds, as well as in Sou hwes Asia. A single Y1 haplo ype is p edominan in no h-cen al Eu ope and a single Y2 haplo ype in cen al Eu ope. In con as , we ound bo h Y1 and Y2 haplo ypes in B i ain, he No dic egion and Russia, wi h he highes Y- ch omosomal di e si y seen in he Ibe ian Peninsula. Conclusions: We p opose ha he homogeneous Y1 and Y2 egions e lec ounde e ec s associa ed wi h he de elopmen and expansion o wo g oups o dai y ca le, he pied o ed b eeds om he No h Sea and Bal ic coas s and he spo ed, yellow o b own b eeds om Swi ze land, espec i ely. The p esen Y1-Y2 con as in cen al Eu ope coincides wi h his o ic, linguis ic, eligious and cul u al bounda ies. Ci a ion: Edwa ds CJ, Ginja C, Kan anen J, Pe ´ ez-Pa dal L, T esse A, e al. (2011) Dual O igins o Dai y Ca le Fa ming – E idence om a Comp ehensi e Su ey o Eu opean Y-Ch omosomal Va ia ion. PLoS ONE 6(1): e15922. doi:10.1371/jou nal.pone.0015922 Edi o : Toomas Ki isild, Uni e si y o Camb idge, Uni ed Kingdom Recei ed Oc obe 12, 2010; Accep ed No embe 29, 2010; Published Janua y 6, 2011 Copy igh : ß2011 Edwa ds e al. This is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed. Funding: CJE was suppo ed by he En e p ise I eland Basic Resea ch G an s P og amme (p ojec numbe s SC/1999/409 and SC/2002/510). CG was suppo ed by a g an om Fundac¸a ˜o Po uguesa pa a a Cie ˆncia e a Tecnologia (Re . SFRH/BD/13502/2003). JK was suppo ed by he Academy o Finland and he Finnish Minis y o Ag icul u e and Fo es y (SUNARE-p og am and ‘Russia in Flux’ p og am). LP-P was suppo ed by g an BES-2006-13545. Collec ion o se e al samples was suppo ed by he Resgen p ojec 98–118 (1999–2002) unded by he Eu opean Union. This wo k was also pa - unded by The Wellcome T us (g an no. 047485/Z/96/Z), and a Eu oco es OMLL P og amme G an ia CNRS, F ance. The unde s had no ole in s udy design, da a collec ion and analysis, decision o publish, o p epa a ion o he manusc ip . Compe ing In e es s: The au ho s ha e decla ed ha no compe ing in e es s exis . * E-mail: [email p o ec ed] ¤ Cu en add ess: Genome Biology and Bioin o ma ics G oup, Hub ech Ins i u e, U ech , The Ne he lands "Fo he ull lis o au ho s o his conso ium, please see he Acknowledgmen s sec ion. In oduc ion The his o y o human ci ilisa ions has le i s oo p in in he pa e ns o gene ic a ia ion o li es ock species ac oss and wi hin con inen s [1,2,3,4]. Molecula ma ke s, such as mi ochond ial DNA (m DNA) and au osomal polymo phisms, ha e been pa icula ly use ul in in es iga ing he wild species o igin o ca le and he subsequen gene ic e en s ha shaped he p esen pa e n o gene ic di e si y. Wi h ega ds o ca le in Eu ope, e idence indica es ha : (i) Balkan ca le ac as ese oi o high gene ic di e si y [5]; (ii) he e is a ma ked con as be ween no h and sou h Eu ope [6,7,8]; and (iii) cen al Eu opean b eeds occupy a sepa a e posi ion ela i e o Medi e anean and no he n Eu opean ca le [9]. Al hough he Fe ile C escen is conside ed he p ima y cen e o au ine ca le domes ica ion, e idence o independen domes ica- ion e en s in o he locals is cu en ly deba ed [10,11,12, 13,14,15]. Ances al au ine m DNA lineages ha e been iden i ied, and con i med di e ences seen be ween no he n and sou he n PLoS ONE | www.plosone.o g 1 Janua y 2011 | Volume 6 | Issue 1 | e15922 Eu opean popula ions o wild ca le (au ochs): he B. p imigenius haplog oup P was equen in no he n and cen al Eu ope [16], while dis inc pu a i e au och ma ilines (haplog oups Q and R) we e ound in mode n sou he n Eu opean popula ions and i appea s ha hese we e spo adically in oduced in o domes ic b eeds [11,12]. M DNA sequences also e eal ha indicine ca le o igina ed om a di e en wild au ochs popula ion, Bos p imigenius namadicus,in he Indus Valley app oxima ely 8,000 yea s be o e p esen [17,18]. Di e en ia ion o pa e nal lineages ia analysis o Y-ch omo- somal a ia ion adds signi ican ly o wha can be in e ed om m DNA and au osomal a ia ion [19]. The absence o in e ch o- mosomal ecombina ion ou side he pseudoau osomal egion (PAR) p ese es o iginal a angemen s o mu a ional e en s, and hus male lineages can be aced bo h wi hin and among popula ions. Gene ic d i is ela i ely s ong due o he e ec i e popula ion sizes o Y-ch omosomes being, a mos , 25% o he au osomal e ec i e popula ion size [20]. E ec i e popula ion size is o en educed u he by he ela i ely high a iabili y o male ep oduc i e success. As a esul , he Y-ch omosome is a sensi i e indica o o ecen demog aphic e en s, such as popula ion bo lenecks, ounde e ec s and popula ion expansions. In se e al he d species, males a e mo e mobile han emales and compe e o ep oduc ion o , in he case o li es ock, a e selec ed on he basis o b eeding objec i es. So while m DNA a ian s s ay mos ly wi hin he he d, Y-ch omosomal a ian s may e lec he o igin o si es as in luenced by in og ession and upg ading. Indeed, in domes ic ca le, a ma ked di e ence be ween he dis ibu ions o mi ochond ial and Y-ch omosomal componen s has been obse ed [16,21,22,23,24]. In an ini ial su ey o Eu opean b eeds, wo haplog oups, Y1 and Y2, we e ound o be dominan in no he n and sou he n Eu ope espec i ely [25]. Compa ison o ca le Y-ch omosome a ia ion o e ime sugges s ha he equency and dis ibu ion o hese pa ilines a ied, which could be ela ed wi h dis inc b eeding s a egies [26]. In Eu opean au ochs, Y2 appea s o be p edominan [27], bu so a i is unclea i he e was signi ican in og ession om wild bulls in o domes ic popula ions. In he s udy o human male lineages, he use o Y-speci ic mic osa elli es has allowed o e ined analyses o he gene ic di e si y o pa e nal lineages ha can be ound wi hin majo haplog oups [28,29]. Simila ly, in ca le, mic osa elli e analysis has iden i ied se e al Y-haplo ypes in Po uguese [30], no he n and eas e n Eu opean [31], wes e n-con inen al, B i ish and Sub- Saha an A ica [14] b eeds, as well as in Ame ican C eole [22] b eeds. E en hough di e en se s o ma ke s we e used in hese s udies, and each only pa ially co e ed he di e si y pa e n o he pa e nal lineages, hey ha e con i med ha Y-ma ke s exhibi a s ong phylogeog aphic s uc u e in ca le. He e we epo Y-haplo ype da a on 128 Eu opean, one A ican and nine Asian b eeds, inco po a ing also da a om he p e ious epo s. This comp ehensi e s udy con i ms a clea no h-sou h con as ha is accen ua ed by a homogenei y o Y1 haplo ypes in no h-cen al Eu ope and o Y2 haplo ypes in and a ound he Alpine egion, bo h egions ha a e hough o be he o igin o highly p oduc i e ca le b eeds. This gene ic bounda y co ela es wi h his o ic di e ences be ween no he n and sou he n Eu opean cul u es and we conside ha his may ha e implica ions o he in es iga ion o dai y QTL a ia ion. Resul s Ca le haplog oups de ined by Y-SNPs Fo 238 males om 30 b eeds, Y-ch omosomal agmen s comp ising he ZFY (1,219 bp and 1,003 bp), SRY (2,644 bp) and DBY (also known as DDX3Y; 406 bp) genes we e sequenced [32]. These sequences con ained i e mu a ional di e ences when compa ed o he zebu Y3 sequences [30], and all Eu opean animals ca ied ei he he Y1 o Y2 au ine haplog oups. In e es ingly, compa ison o he Y3 sequence wi h an SRY sequence om an Indian Sahiwal zebu (GenBank accession numbe AY079145) [33] e ealed h ee addi ional di e ences downs eam o he open- eading ame, indica ing zebu-speci ic Y-ch omosomal SNPs. In combina ion wi h a SNP in UYT19 [14,22,25,31], h ee coseg ega - ing mu a ions di e en ia e he au ine Y1 and Y2 haplog oups (Table S1). A composi e mic osa elli e in DBY [25], wi h one majo allele in bo h Y1 and Y2 and only p esen in he I alian Ma emmana, was no used o di e en ia ion o haplo ypes. Geno ypes o indi idual SNPs in o he animals we e combined wi h Y1-Y2 SNP da a and esul ed in Y1 o Y2 assignmen s o 2087 animals om 138 b eeds (Table S1). The esul ing da ase included p e iously published geno ypic in o ma ion o 1099 indi iduals om 78 b eeds [14,22,31]. The Y3 haplog oup was iden i ied on he basis o mic osa elli e in o ma ion as desc ibed in he nex sec ion. The map o Figu e 1 shows he geog aphical dis ibu ion o Y-haplog oups. The h ee haplog oups desc ibed in ca le (Y1, Y2 and Y3) we e de ec ed in Sou hwes Asia, bu only Y3 was p esen in he wo Indian b eeds analysed, which is in ag eemen wi h hei zebu mo phology. Y1 was p edominan in no he n Eu ope and in a numbe o Ibe ian b eeds. In con as , Y2 was dominan in mos cen al, Medi e anean and Ibe ian b eeds, bu was also ound in se e al B i ish and No dic b eeds. Al hough only a single A ican b eed was included in his s udy, bo h Y1 and Y2 haplog oups we e p esen . Se e al o he b eeds ha do no con i m his no he n Y1 – sou he n Y2 dis ibu ion pa e n appea o ha e been subjec o ecen in og ession om b eeds wi h simila coa colou [34], bu ca ying he o he Y-ch omosomal haplog oup. Thus, Y2 was in oduced in Du ch Bel ed (DUB) by c ossb eeding wi h bel ed Galloway bulls. Danish Red bulls p obably in oduced Y1 in o he Sicilian Modicana (MOD). The p esence o Y1 in cen al dai y b eeds, such as Simmen al (SIM), Pezza a Rossa I aliana (PRI) and Hinde wald (HIW), is p obably explained by c ossb eeding wi h Red Hols ein si es. Likewise, c ossb eeding wi h Lowland Pied o English ca le p obably accoun s o he p edominance o Y1 in Russian dai y ca le [35]. Y-ch omosomes ac as a single haplog oup and a e, in gene al, homogeneous a he Y- ch omosome a ia ion le el. In mos cases, he p esence o Y1 and Y2 haplo ypes in a gi en b eed can be explained by i s ecen his o y [14]. Ca le haplo ypes de ec ed h ough SNPs and mic osa elli es The di e si y wi hin each haplog oup was u he assessed by geno yping INRA189 [36] and BM861 [37] Y-speci ic mic osa - elli e ma ke s. The combina ion o hese da a wi h p e iously published Y-ch omosomal haplo ypes [14,22,31] yielded haplo- ypes o a o al o 1472 animals om 111 b eeds, a subse o he indi iduals o which SNP in o ma ion was a ailable. Haplo ype composi ion and absolu e equencies, as well as unbiased es ima es o haplo ype di e si ies wi h he associa ed s anda d de ia ions (SD) a e shown o each b eed and geog aphic g oup in Table 1. We ound a o al o 19 composi e Y-haplo ypes. The ela ionship be ween cu en haplo ype nomencla u es is summa- ised in Table S2. Locus INRA189 is he mos in o ma i e ma ke wi h 10 alleles, di e en ia ed among i e Y1 and nine Y2 haplo ypes. Fo 21 bulls belonging o he Indian and Sou hwes Asian b eed g oups, haplog oup Y3 was iden i ied ia he INRA189-88 bp allele. Mic osa elli e ma ke BM861 de ines one Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 2 Janua y 2011 | Volume 6 | Issue 1 | e15922 addi ional Y1 and h ee Y2 addi ional haplo ypes. Haplo ype Y1- 98-158 is he mos equen wi hin he Y1 haplog oup and is de ec ed in 82% o he animals om his haplog oup ac oss all geog aphic b eed g oups wi h he excep ion o he Indian and Podolian. Wi hin he Y2 haplog oup, Y2-102-158 and Y2-104- 158 haplo ypes accoun o 62% and 29% o he animals espec i ely. A map showing he dis ibu ion o Y-haplo ypes is included in Figu e S1. Y-ch omosomal di e si y wi hin b eeds is low (mean o 0.4260.3) wi h ixed haplo ypes in 65 ou o 111 b eeds (app oxima ely 59%). In e es ingly, he Sou hwes Asian b eed g oup is he mos gene ically di e se, wi h a o al o se en haplo ypes de ec ed in a limi ed sample o 24 animals, and an unbiased expec ed haplo ype di e si y o 0.5760.4 (Table 2). The Ibe ian and B i ish g oups ha e in e media e a iabili y, wi h 11 and i e haplo ypes obse ed and di e si ies o 0.3460.2 and 0.4160.3 espec i ely. Phylogeog aphy o Y-haplo ypes The phylogene ic ela ionship among Y-haplo ypes was in es- iga ed a e g ouping he b eeds in o 12 egions on he basis o geog aphy and/o pheno ype [34,38]. These b eed g oups a e in ag eemen wi h majo clus e s as de ined by au osomal mic osa - elli e (unpublished esul s; see also Figu e S2) and SNP da a [7]. Haplo ype ela ionships a e depic ed in Figu e 2 by a median- joining (MJ) ne wo k ob ained o he comple e da ase , as well as by egional MJ ne wo ks de ined o each o he 12 geog aphic b eed g oups. The MJ ne wo ks clea ly di e en ia e he indicine Y3 pa iline om he au ine Y1 and Y2 haplog oups. The egional ne wo ks depic he Y-ch omosome di e si y ound in each egion and he ela ionship among he obse ed haplo ypes de ined by he wo mic osa elli es. AMOVA esul s a e p esen ed in Table S3 and show a signi ican (P,0.0001) e ec o geog aphical b eed g ouping, which accoun ed o 31% o he o al a iabili y. App oxima ely 51% (P,0.0001) o he Y-ch omosome gene ic a ia ion was ound among b eeds wi hin g oups and 18% (P,0.0001) wi hin b eeds. This was con i med by he gene ally high Y-ch omosomal FST alues (Table S4) o all pai wise b eed clus e s, which we e low mainly o he compa ison o he dai y no h-wes e n Eu opean b eed clus e s. In Figu e S2, Y-ch omosomal haplo ypes ha e been indica ed in a Neighbo Ne phylogene ic ne wo k o Reynolds’ dis ances based on 30 au osomal mic osa elli e da a. This shows a clea consis ency be ween Y-ch omosomal a ia ion and he b eed ela ionships in he au osomal-based phylogeny, wi h only he B i ish Y2 and Ibe ian Y1 ca le as majo excep ions [as in 14,15]. Discussion Di e en ia ion o pa e nal lineages in Eu opean ca le We analysed Y-ch omosomal haplo ypes in a comp ehensi e sampling o Eu opean ca le. This allowed a di e en ia ion o wo SNP-based au ine haplog oups, which we e esol ed in o 18 haplo ypes using geno ypes om wo mic osa elli e ma ke s. Locus INRA189 appea ed o be, by a , he mos in o ma i e and, in combina ion wi h he o he ma ke and SNPs, showed ha pa e nal lineages s ongly depend on geog aphic o igin. A u he di e en ia ion was demons a ed by using o he mic osa elli es [14,22,31]. Fo ins ance, BYM1 alleles de ined a Y1-98-158 a ian in No dic ca le and a Y2-102-158 a ian in Spain [14], while DYZ1 de ec ed a di e en Y2-102-158 a ian in Sou hwes Asian b eeds [31]. Dis ibu ion o zebu and au ine haplo ypes P e ious gene ic s udies ha e demons a ed a sepa a ion o he mi ochond ial [39,40,41], Y-ch omosomal [25,42,43] and nuclea [21] DNA om au ine and zebu ca le, which suppo s independen domes ica ions in he Fe ile C escen and Indus alley espec i ely [44]. In a di e se panel o 2009 Eu opean ca le, we exclusi ely ound au ine Y-ch omosomal haplo ypes. Figu e 1. Geog aphical dis ibu ion o Y-haplog oups. (a) Eu ope, and (b) Eu asia. G een = Y1; ed = Y2; black = Y3. Abb e ia ions o b eed names a e gi en in Table 1. doi:10.1371/jou nal.pone.0015922.g001 Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 3 Janua y 2011 | Volume 6 | Issue 1 | e15922 Table 1. B eed in o ma ion, including geog aphical g ouping, o he 111 ca le b eeds sampled as pa o his s udy, and associa ed haplo ypic da a (de ined as SNP-INRA189- BM861) and di e si y alues. Geog aphic g ouping B eed Code Coun y o o igin Numbe o Y-ch omo- somes Haplo ype haplo ype di e si y (±SD) o al numbe o haplo ypes Y1-94-158 Y1-96-158 Y1-98-158 Y1-98-160 Y1-100-158 Y1-102-158 Y2-80-158 Y2-90-158 Y2-94-158 Y2-96-158 Y2-98-158 Y2-98-160 Y2-100-158 Y2-102-158 Y2-102-160 Y2-104-158 Y2-104-160 Y2-106-158 Y3-88-156 India (IND) Nello e NEL B azil 12 12 0.00060.000 1 Ongole ONG India 4 4 0.00060.000 1 To al 16 16 0.000±0.000 1 A ica (AFR) N’Dama NDM Guinea 12 2 9 1 0.24760.184 3 To al 12 2 9 1 0.247±0.184 3 Sou hwes Asia (SWA) Ana olian Black ANT Tu key 5 1 1 2 1 0.30060.424 4 Damascus DAM Sy ia 3 1 1 1 0.55660.416 3 Eas Ana olian Red EAR Tu key 4 1 2 1 0.27860.393 3 Middle I aqi IQM I aq 4 3 1 0.50060.000 2 No h I aqi IQN I aq 1 1 n/a 1 Sou h I aqi IQS I aq 3 3 0.00060.000 1 Sou h Ana olian Red SAR Tu key 4 2 2 0.22260.314 2 To al 24 4 1 1 1 7 5 5 0.574±0.192 7 Podolian (POD) Chianina CHI I aly 20 20 0.00060.000 1 Is ian IST C oa ia 4 4 0.00060.000 1 Ma chigiana MCG I aly 11 11 0.00060.000 1 Ma emmana MMA I aly 19 19 0.00060.000 1 Podolica PODi I aly 13 9 4 0.15460.218 2 Se bian Podolica PODs Se bia 4 4 0.00060.000 1 Tu kish G ey TGY Tu key 3 3 0.00060.000 1 Uk ainian G ey UGY Uk aine 5 5 0.00060.000 1 Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 4 Janua y 2011 | Volume 6 | Issue 1 | e15922 Geog aphic g ouping B eed Code Coun y o o igin Numbe o Y-ch omo- somes Haplo ype haplo ype di e si y (±SD) o al numbe o haplo ypes Y1-94-158 Y1-96-158 Y1-98-158 Y1-98-160 Y1-100-158 Y1-102-158 Y2-80-158 Y2-90-158 Y2-94-158 Y2-96-158 Y2-98-158 Y2-98-160 Y2-100-158 Y2-102-158 Y2-102-160 Y2-104-158 Y2-104-160 Y2-106-158 Y3-88-156 To al 79 5 28 43 3 0.193±0.273 4 Ibe ian (IBE) Alen ejana ALN Po ugal 34 34 0.00060.000 1 Alis ana- Sanab esa ALS Spain 12 12 0.00060.000 1 A ouquesa ARQ Po ugal 33 25 8 0.12660.179 2 As u iana de los Valles ASV Spain 38 26 6 6 0.25660.202 3 As u iana de Mon ana ASM Spain 19 18 1 0.07060.050 2 A ilena Neg o Ibe ica AVI Spain 7 1 1 5 0.27060.214 3 Ba osa ˜BAR Po ugal 33 4 29 0.07360.104 2 Be enda BER Spain 5 3 2 0.20060.283 2 Be izu BEB Spain 17 17 0.00060.000 1 B a a de Lide BRV Po ugal 26 2 23 1 0.12260.091 3 Cachena CCH Po ugal 25 1 24 0.02760.038 2 Ga onesa GAR Po ugal 6 6 0.00060.000 1 Lidia LID Spain 66 1 1 64 0.02060.028 3 Mallo quina MAL Spain 8 8 0.00060.000 1 Ma inhoa MAH Po ugal 17 17 0.00060.000 1 Ma onesa MAR Po ugal 23 23 0.00060.000 1 Me olenga MRT Po ugal 21 7 1 1 2 10 0.37860.273 5 Minho a MIN Po ugal 28 28 0.00060.000 1 Mi andesa MIR Po ugal 23 23 0.00060.000 1 Mo ucha MOR Spain 5 5 0.00060.000 1 Mos enca MOS Spain 21 21 0.00060.000 1 Pajuna PAJ Spain 4 1 2 1 0.44460.342 3 P e a PRT Po ugal 29 1 1 5 22 0.15860.178 4 Re in a RET Spain 6 4 2 0.17860.251 2 Rubia Gallega RGA Spain 44 44 0.00060.000 1 Sayaguesa SAY Spain 8 1 5 2 0.20260.286 3 Table 1. Con . Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 5 Janua y 2011 | Volume 6 | Issue 1 | e15922 Geog aphic g ouping B eed Code Coun y o o igin Numbe o Y-ch omo- somes Haplo ype haplo ype di e si y (±SD) o al numbe o haplo ypes Y1-94-158 Y1-96-158 Y1-98-158 Y1-98-160 Y1-100-158 Y1-102-158 Y2-80-158 Y2-90-158 Y2-94-158 Y2-96-158 Y2-98-158 Y2-98-160 Y2-100-158 Y2-102-158 Y2-102-160 Y2-104-158 Y2-104-160 Y2-106-158 Y3-88-156 Tudanca TUD Spain 10 10 0.00060.000 1 To al 568 44 57 1 1 1 1 1 277 17 140 28 0.335±0.244 11 Cen al (CEN) Blonde d’Aqui aine BDA F ance 5 3 2 0.20060.283 2 B una de los Pi ineds BPI Spain 11 11 0.00060.000 1 Busha BUS Se bia 5 5 0.00060.000 1 Cabannina CAB I aly 2 1 1 0.33360.471 2 Cha olais CHA F ance 31 30 1 0.02260.030 2 Limousin LIM F ance 24 24 0.00060.000 1 Mon belia d MBE F ance 6 6 0.00060.000 1 Pa henaise PAR F ance 15 4 11 0.27960.198 2 Piemon ese PIM I aly 13 2 11 0.09460.133 2 Pinzgau PGZ Aus ia 9 9 0.00060.000 1 Pi enaica PIR Spain 10 8 2 0.11960.168 2 Pus e ale PUS I aly 13 13 0.00060.000 1 Sale s SAL F ance 20 1 19 0.06760.047 2 Simmen al SIM Swi ze - land 15 15 0.00060.000 1 Swiss B own SWB Swi ze - land 14 14 0.00060.000 1 Ta en aise TAR F ance 18 18 0.00060.000 1 Ty olean G ey TYG I aly 19 2 17 0.06660.094 2 To al 230 5 4 215 1 5 0.056±0.045 5 B i ish (BRT) Abe deen Angus ABA Sco land 27 20 7 0.13360.188 2 Ay shi e AYR Sco land 16 16 0.00060.000 1 B i ish Whi e BWH England 21 16 1 1 3 0.25260.111 4 Dex e DEX I eland 4 4 0.00060.000 1 Galloway GAL Sco land 9 9 0.00060.000 1 He e o d HER England 21 20 1 0.06360.045 2 Highland HIG Sco land 10 10 0.00060.000 1 Je sey JER Je sey 19 19 0.00060.000 1 To al 127 56 8 20 21 22 0.413±0.226 5 Table 1. Con . Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 6 Janua y 2011 | Volume 6 | Issue 1 | e15922 Geog aphic g ouping B eed Code Coun y o o igin Numbe o Y-ch omo- somes Haplo ype haplo ype di e si y (±SD) o al numbe o haplo ypes Y1-94-158 Y1-96-158 Y1-98-158 Y1-98-160 Y1-100-158 Y1-102-158 Y2-80-158 Y2-90-158 Y2-94-158 Y2-96-158 Y2-98-158 Y2-98-160 Y2-100-158 Y2-102-158 Y2-102-160 Y2-104-158 Y2-104-160 Y2-106-158 Y3-88-156 No dic (NOR) Blacksided T oende STN No way 7 7 0.00060.000 1 Doela DOL No way 4 4 0.00060.000 1 Eas e n Finnca le EFC Finland 9 1 8 0.14860.105 2 Eas e n Red Polled ORA No way 5 5 0.00060.000 1 Fjallna a FNR Sweden 3 3 0.00060.000 1 Icelandic ICL Iceland 8 8 0.00060.000 1 No he n Finnca le NFC Finland 3 3 0.00060.000 1 No wegian (comme cial, hyb id) NRF No way 12 12 0.00060.000 1 Swedish Moun ain SFR Sweden 8 8 0.00060.000 1 Swedish Red Polled ROK Sweden 3 3 0.00060.000 1 Telema k TEL No way 2 2 0.00060.000 1 Wes e n Finnca le WFC Finland 9 9 0.00060.000 1 Wes e n Fjo d VFJ No way 6 3 3 0.20060.283 2 Wes e n Red Polled VRA No way 3 2 1 0.22260.314 2 To al 82 64 4 6 8 0.222±0.161 4 Bal ic Red (BHR) Angle ANG Ge many 10 10 0.00060.000 1 Danish Red RDM Denma k 19 18 1 0.07060.050 2 La ian Blue (na i e) LBL La ia 9 9 0.00060.000 1 La ian B own (comme cial) LBR La ia 8 8 0.00060.000 1 La ian Danish Red DAR La ia 7 3 4 0.38160.269 2 Suksunskaya SUK Russia 5 4 1 0.26760.189 2 Uk ainian Red S eppe RST Uk aine 5 1 4 0.13360.189 2 To al 63 1 56 6 0.126±0.090 3 Table 1. Con . Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 7 Janua y 2011 | Volume 6 | Issue 1 | e15922 Geog aphic g ouping B eed Code Coun y o o igin Numbe o Y-ch omo- somes Haplo ype haplo ype di e si y (±SD) o al numbe o haplo ypes Y1-94-158 Y1-96-158 Y1-98-158 Y1-98-160 Y1-100-158 Y1-102-158 Y2-80-158 Y2-90-158 Y2-94-158 Y2-96-158 Y2-98-158 Y2-98-160 Y2-100-158 Y2-102-158 Y2-102-160 Y2-104-158 Y2-104-160 Y2-106-158 Y3-88-156 No h-Wes (NWE) Belgian Blue BWB F ance 21 19 2 0.06060.085 2 Belgian Red BRE Belgium 4 4 0.00060.000 1 No mand NOR F ance 46 46 0.00060.000 1 Sho ho n SHN Belgium 19 19 0.00060.000 1 To al 90 19 71 0.112±0.159 2 Lowland Pied (LLP) Du ch Bel ed DUB Ne he lands 8 3 5 0.35760.253 2 F iesian-Du ch FRH Ne he lands 8 8 0.00060.000 1 Ge man O iginal Black Pied-Wes BPW Ge many 3 3 0.00060.000 1 G oningen Whi ehead GWH Ne he lands 6 6 0.00060.000 1 Hols ein F iesian HFR Ne he lands 65 64 1 0.02160.015 2 Ju land (old na i e) SJM Denma k 6 6 0.00060.000 1 Meuse-Rhine- Yssel MRY Ne he lands 9 9 0.00060.000 1 Red Hols ein dual ype RH2 Ne he lands 1 1 n/a 1 To al 106 100 1 5 0.072±0.039 3 Eas e n (EAS) Bes uzhe BZH Russia 4 4 0.00060.000 1 Is obenskaya ISB Russia 9 9 0.00060.000 1 Kalmyk KAL Russia 12 12 0.00060.000 1 Kholomo- go skaya KHO Russia 6 6 0.00060.000 1 Pecho skaya PCH Russia 7 7 0.00060.000 1 Uk ainian Whi eheaded UWH Uk aine 11 4 1 6 0.38860.276 3 Yaku ian ca le YKT Sibe ia 23 22 1 0.02960.041 2 Ya osla skaya YAR Russia 3 3 0.00060.000 1 To al 75 33 1 6 34 1 0.373±0.247 5 O e all 111 b eeds 1472 44 20 448 8 25 1 6 14 1 1 2 1 7 559 18 259 1 36 21 0.422±0.269 doi:10.1371/jou nal.pone.0015922. 001 Table 1. Con . Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 8 Janua y 2011 | Volume 6 | Issue 1 | e15922 This implies ha he zebu alleles ound o au osomal ma ke s in he Podolian [6,45,46,47], Ibe ian [6,48,49] and Uk ainian Whi ehead [31] b eeds came o Eu ope indi ec ly, p esumably ia Ana olia, No h A ica o no h o he Black Sea. In addi ion, he p esence o zebu Y-ch omosomes in Sou hwes Asia indica e ha zebu in og ession only ook place a e he expansion o domes ic au ine ca le om Sou hwes Asia owa ds Eu ope [16]. Tau ine haplog oups The di e gence o he wo haplog oups Y1 and he Y2 wi hou in e media e haplo ypes sugges s ha domes ica ion combined pa e nal lineages o igina e om wo di e ged popula ions. Rema kably, bo h haplog oups we e ound in Sou hwes Asia. In Eu ope, he Y1 and Y2 haplog oups ound in ex an ca le exhibi a clea geog aphic s uc u e, wi h Y1 es ic ed o no he n Eu opean and Ibe ian b eeds. Ini ially, his was explained by local au ochs in og ession, supposed o ca y he Y1 lineage [25]; howe e , his does no accoun o he p esence o Y1 in Sou hwes Asia. In addi ion, a subsequen s udy [27] exclusi ely ound Y2 haplog oups in Eu opean au ochs. We no e ha his does no exclude ha he Y2 lineage was pa ially con ibu ed by local au ochs, no ha condi ions o Neoli hic a ming may ha e c ea ed oppo uni ies o male in og ession om wild animals. Howe e , se e al analyses o m DNA ha e clea ly demons a ed ha domes ic ma e nal lineages o igina e om Sou hwes Asia, wi h only spo adic emale au ochs in og ession [11,12,16,50,51]. An ob ious possibili y is ha he cu en Y-ch omosomal haplog oup dis ibu ion e lec s Neoli hic immig a ion ou es. Acco ding o a chaeological e idence, he dispe sal o ag icul u e in Eu ope s a ed in G eece a ound 7,000 BC, mo ed o sou he n I aly ci ca. 6,000 BC, and hen along a sou he n ou e in o he wes e n Medi e anean be ween 5,600 and 5,400 BC, eaching Po ugal a ound 5,300 BC. Mig a ion along he con inen al ou e in o Poland and Ge many occu ed be ween 5,500 and 5,300 BC, eaching no h-wes e n F ance a ound 5,000 BC; sou he n Scandina ia, he B i ish Isles and I eland we e eached ci ca.o a e 4,000 BC [52,53,54]. I is gene ally accep ed ha ag icul u e sp ead ia hese wo ou es: he Medi e anean ou e and he Danubian (o con inen al) ou e. Al hough Y1 has a clea p esence in Ibe ian ca le, Y2 pa e nal lineages domina e in he p esen Medi e anean a ea. A ounde e ec in Danubian immig an s could ha e caused he dominance o Y1 in no he n Eu ope. In his scena io, he p esence o Y1 in Ibe ia would ha e esul ed om mo emen s along he A lan ic seaboa d, as documen ed by he Neoli hic a chaeological eco d [55], and he p esence o wo haplog oups in B i ain may indica e a con e gence o immig an s o bo h ou es. Al e na i ely, colonisa ion o B i ain may ha e p eda ed he expansion o Y1, which could ha e a i ed in B i ain la e ia he documen ed impo o Du ch si es in he 18 h cen u y. This would be in line wi h analysis o skele al emains exca a ed in Sweden, showing ha Y1 bulls eplaced Y2 bulls du ing o a e he la e Middle Ages [26], al hough Y1 ca le we e aken o Iceland by he Vikings c. 1,000 AD. Howe e , a Y1 ounde e ec , long a e he in oduc ion o domes ic ca le in no he n Eu ope, is he mos consis en wi h he haplo ype di e si y pa e n. Y1 samples iden i ied in A ica a e mo e likely o be he esul o a ecen in og ession o Eu opean ca le a he han he expansion o a gene ically he e ogeneous si e popula ion domes- ica ed in he Fe ile C escen . Y-speci ic mic osa elli e da a con i m he exis ence o a Y2 haplo ypic sub amily in A ican ca le es ic ed o he A ican con inen [14,15]. Dis ibu ion o haplo ype di e si y The comp ehensi e co e age o ou s udy pe mi s a compa ison o he di e si y o pa e nal lineages in di e en egions. E en in a limi ed sampling, Sou hwes Asian ca le con ain se en ou o he 19 au ine haplo ypes iden i ied in his s udy. This suppo s he heo y ha he Fe ile C escen was a majo cen e o ca le domes ica ion and ha Eu opean ca le a e a subse o an ini ially di e se Sou hwes Asian domes ic popula ion. The high di e si y in Spain and Po ugal is p obably explained by he isola ed posi ion o he Ibe ian Peninsula, by which much o he o iginal di e si y has been conse ed. Howe e , he inc eased di e si y may also ha e been in luenced by A ican in og ession, which is consis en wi h mi ochond ial and au osomal in o ma ion Table 2. Haplo ypic da a o he b eeds yped o he Y1-Y2-Y3 SNPs and he wo mic osa elli e loci, INRA189 and BM861. Geog aphic g ouping SNPs Mean numbe o samples / b eed Mic osa elli es Mean numbe o samples / b eed To al numbe o haplo ypes Haplo ype di e si y (±SD) B eeds Samples B eeds Samples India (IND) 2 16 8.0 2 16 8.0 1 0.00060.0 A ica (AFR) 1 14 n/a 1 12 n/a 3 0.24760.2 Sou hwes Asia (SWA) 7 25 3.6 7 24 3.4 7 0.57460.4 Podolian (POD) 12 184 15.3 8 79 9.9 4 0.19360.2 Ibe ian (IBE) 31 651 21.0 27 568 21.0 11 0.33560.2 Cen al (CEN) 30 453 15.1 17 230 13.5 5 0.05660.1 B i ish (BRT) 10 164 16.4 8 127 15.9 5 0.41360.3 No dic (NOR) 14 95 6.8 14 82 5.9 4 0.22260.2 Bal ic Red (BHR) 9 77 8.6 7 63 9.0 3 0.12660.1 No h-Wes (NWE) 5 126 25.2 4 90 22.5 2 0.11260.1 Lowland Pied (LLP) 9 208 23.1 8 106 13.3 3 0.07260.1 Eas e n (EAS) 8 74 9.3 8 75 9.4 5 0.37360.3 O e all 138 2087 15.1 111 1472 13.3 19 0.422±0.3 doi:10.1371/jou nal.pone.0015922. 002 Y-Haplo ype Dis ibu ion in Eu opean Ca le PLoS ONE | www.plosone.o g 9 Janua y 2011 | Volume 6 | Issue 1 | e15922