Meta-analysis of mitochondrial DNA reveals several population bottlenecks during worldwide migrations of cattle

Di e si y 2014, 6, 178-187; doi:10.3390/d6010178 di e si y ISSN 1424-2818 www.mdpi.com/jou nal/di e si y Communica ion Me a-Analysis o Mi ochond ial DNA Re eals Se e al Popula ion Bo lenecks du ing Wo ldwide Mig a ions o Ca le Johannes A. Lens a 1,*, Paolo Ajmone-Ma san 2, Albano Beja-Pe ei a 3, Ru h Bollongino 4, Daniel G. B adley 5, Licia Colli 2, Anna De Gae ano 6, Cei idwen J. Edwa ds 5,7, Ma leen Felius 8, Luca Fe e i 6, Ca a ina Ginja 9, Pe e H is o 10, Juha Kan anen 11, Juan Ped o Li ón 12, Da id A. Magee 5,13, Ricca do Neg ini 2 and Geo gi A. Radosla o 10 1 Facul y o Ve e ina y Medicine, U ech Uni e si y, Yalelaan 104, U ech 3584CM, The Ne he lands 2 Uni e si à Ca olica del Sac o Cuo e, Ins i u e o Zoo echnics and BioDNA-Biodi e si y and Ancien DNA Resea ch Cen e , Via Emilia Pa mense 84, Piacenza 29122, I aly; E-Mails: [email p o ec ed] (P.A.-M.); licia.colli@unica .i (L.C.); icca do[email p o ec ed] (R.N.) 3 Cen o de In es igação em Biodi e sidade e Recu sos Gené icos da Uni e sidade do Po o (CIBIO/UP), Campus Ag á io de Vai ão, Rua Pad e A mando Quin as 7, Vai ão 4485-661, Po ugal; E-Mail: [email p o ec ed] 4 Ins i u e o An h opology, Johannes-Gu enbe g Uni e si y Mainz, Anselm-F anz- on-Ben zel-Weg 7, Mainz 55128, Ge many; E-Mail: [email p o ec ed] 5 Smu i Ins i u e o Gene ics, T ini y College, Dublin 2, I eland; E-Mail: db adley@ cd.ie 6 Dipa imen o di Biologia e Bio ecnologie “L. Spallanzani”, Uni e si à di Pa ia, Pa ia 27100, I aly; E-Mail: [email p o ec ed] (A.D.G.); luca. [email p o ec ed] (L.F.) 7 Resea ch Labo a o y o A chaeology, Uni e si y o Ox o d, Dyson Pe ins Building, Sou h Pa ks Road, Ox o d OX1 3QY, UK; E-Mail: [email p o ec ed] 8 Mau i ss aa 167, Ro e dam 3012 CH, The Ne he lands; E-Mail: [email p o ec ed] 9 Cen o de Biologia Ambien al, Faculdade de Ciências, Uni e sidade de Lisboa, Lisboa 1749-016, Po ugal; E-Mail: [email p o ec ed] 10 Bulga ian Academy o Sciences, Ins i u e o Biodi e si y and Ecosys em Resea ch, “Acad. Geo gi Bonche ” s ., bl. 25, So ia 1113, Bulga ia; E-Mails: pe[email p o ec ed] (P.H.); [email p o ec ed] (G.A.R.) 11 Bio echnology and Food Resea ch, MTT Ag i ood Resea ch Finland, Jokioinen, Finland and Depa men o Biology, Uni e si y o Eas e n Finland, P.O. Box 1627, FI-70211 Kuopio, Finland; E-Mail: juha.kan anen@m . i 12 CIGEBA, Facul ad de Ciencias Ve e ina ias, Uni e sidad Nacional de La Pla a, Calle 60 y 118 s/n, La Pla a, Buenos Ai es 1900, A gen ina; E-Mail: [email p o ec ed] 13 Animal Genomics Labo a o y, UCD School o Ag icul u e and Food Science, Uni e si y College Dublin, Bel ield, Dublin 4, I eland; E-Mail: [email p o ec ed] OPEN ACCESS Di e si y 2014, 6 179 * Au ho o whom co espondence should be add essed; E-Mail: [email p o ec ed]; Tel.: +31-30-253-4992; Fax: +31-31-253-5077. Recei ed: 13 Janua y 2014; in e ised o m: 26 Feb ua y 2014 / Accep ed: 28 Feb ua y 2014 / Published: 14 Ma ch 2014 Abs ac : Se e al s udies ha e in es iga ed he di e en ia ion o mi ochond ial DNA in Eu asian, A ican and Ame ican ca le as well as a chaeological bo ine ma e ial. A global su ey o hese s udies shows ha haplog oup dis ibu ions a e mo e s able in ime han in space. All majo mig a ions o ca le ha e shi ed he haplog oup dis ibu ions conside ably wi h a educ ion o he numbe o haplog oups and/o an expansion o haplo ypes ha a e a e o absen in he ances al popula ions. The mos ex eme case is he almos exclusi e coloniza ion o A ica by he T1 haplog oup, which is a e in Sou hwes Asian ca le. In con as , ancien samples in a iably show con inui y wi h p esen -day ca le om he same loca ion. These indings indica e s ong ma e nal ounde e ec s ollowed by limi ed ma e nal gene low when new e i o ies a e colonized. Howe e , e ec s o adap a ion o new en i onmen s may also play a ole. Keywo ds: ca le; b eeds; mi ochond ial DNA; haplog oups; mig a ions 1. In oduc ion Du ing he pas decades, analysis o mi ochond ial DNA (m DNA) has become he backbone o molecula -gene ic in es iga ions o animal popula ion di e si y and his o y [1]. Due o i s high a iabili y, in o ma i e da ase s can be collec ed ela i ely as , while i s high copy numbe inc eases he chance o e ie ing DNA om a chaeological ma e ial. In addi ion, he in e p e a ion o m DNA da ase s is acili a ed by ma e nal ansmission and absence o ecombina ion; he la e gene a ing a s aigh o wa d hie a chical clus e ing [2]. Fo se e al li es ock species, m DNA analyses es ablished he ances al species and con ibu ed o e idence o he localiza ion o domes ica ion si es [3]. The inding o wo sepa a e domes ica ion e en s, one o au ine (Bos au us) and one o zebu (Bos indicus) ca le [4,5], co esponded wi h he a chaeological eco d. The exclusi e p esence o au ine m DNA in A ican zebu [4] indica ed ha zebu was in oduced in o A ica by male in og ession alone and demons a ed he unique con ibu ion o m DNA analysis o he econs uc ion o ag icul u al his o y. Since hen, nume ous s udies ha e explo ed he mi ochond ial di e si y o ca le popula ions wo ldwide (Table S1). Fi e au ine (T) and wo indicine (I) haplog oups accoun o he as majo i y o m DNA haplo ypes [6–9]. Comple e m DNA sequences ha e es ablished an accu a e phylogeny and indica ed a Sou hwes -Asian o igin o all majo T haplog oups, including he A ican T1 and Eas -Asian T4 [10,11]. These and o he s udies also iden i ied he a e haplog oups P, Q and R, wi h P and R mos likely de i ed om Eu opean au ochs [12–14]. Focusing on he majo haplog oups, we combined he esul s o se e al egional s udies o he ca le m DNA con ol egion (Table S1). This global me a-analysis allows a ew gene aliza ions abou shi s Di e si y 2014, 6 180 in haplog oup dis ibu ions, sugges ing s ong ounde e ec s du ing coloniza ion o Eu ope, Eas Asia, A ica and Ame ica, bu li le empo al a ia ion. 2. Expe imen al Sec ion Table S1 shows he sou ces o ca le m DNA da ase s used in his s udy wi h a o al o 6695 D-loop sequences. The haplog oups T, T1, T2, T3 and T4 could be di e en ia ed by a ia ion wi hin a 240-bp D-loop segmen [6,8,9,12]. In his s udy haplog oup T deno es he combina ion o T, T1’2’3 and T5. Haplog oup coun s we e aken di ec ly om publica ions o based on haplo ype sco ing o epo ed GenBank en ies. 3. Resul s and Discussion A wo ldwide geog aphic plo o haplog oup dis ibu ions (Figu e 1) isualizes se e al spa ial con as s. T oy e al. [6] al eady no ed he high haplog oup di e si y in Sou hwes Asia wi h ou majo haplog oups T, T1, T2 and T3, he dominance o haplog oup T3 in Eu ope and he almos exclusi e occu ence o T1 in A ica. A ecen analysis o Neoli hic samples om I an e ealed he same haplog oup di e si y as obse ed in p esen Sou hwes Asian ca le [15], while T3 was al eady p edominan in Cen al and No hwes e n Eu ope du ing he Neoli hic [16–23] (Figu e 2). The combina ion o da a om se e al sou ces now sugges s ha he en y o ca le in o Eu ope ca. 8,500 BP la gely educed he equency o haplog oups T and T1. Haplog oup T2 s ill has app eciable equencies in I alian, Balkan and Asian au ine ca le, bu is ound only spo adically in Cen al, Wes e n and No he n Eu ope. The p esence o T1 in he Ibe ian peninsula sugges s p ehis o ic and/o la e A ican in luence [19,24,25]. This is also he mos likely explana ion o a simila equency o T1 in he Podolian b eeds om Sicily and Sou h I aly. The ma e nal lineages in Cen al-I alian la ge whi e and Podolian ca le (Chianina, Ma emmana, Romagnola, Ma chigiana), wi h equencies o bo h T1 and T2 o a ound 10%, a e in e media e be ween hose o he Sou h-I alian and Balkan Podolian ca le. Thus, a p oposed Ana olian o igin o ma e nal lineages om Tuscany by immig a ion o ca le well a e he Neoli hic coloniza ion o I aly [26] can be ex ended o neighbo ing Podolian b eeds. A gene ic link be ween m DNA om Ana olian and I alian ca le, implying anspo o cows, may ha e been media ed by he Tuscans [26] and/o co espond o he documen ed impo since he 8 h cen u y BC o la ge ca le om Epi us (p esen Sou h Albania-No hwes G eece) o I aly [27]. In A ica, haplo ypes om haplog oups o he han T1 ha e been ound only in Egyp (combined equency 38.5%) and No hwes A ica (less han 2%) and a e comple ely absen in he es o he con inen . A ecen comp ehensi e s udy o whole m DNA o he T1 haplog oup iden i ied eigh haplo ypes as ounde s o he A ican T1 popula ion [11]. Es ima es o coalescence imes o he T1 sub-haplog oups (6,200 o 12,900 BP) and hei cu en geog aphic dis ibu ions a e compa ible wi h a Sou hwes -Asian o igin o mos T1 sub-haplog oups, which o sub-haplog oup T1c1 has been con i med by i disco e y in I aq [14]. I is no clea ye how o explain he o e ep esen a ion in A ica o di e en sub-haplog oups exclusi ely om he T1 haplog oup. Possible explana ions include posi i e selec ion o T1 m DNA (see below), inhe en unce ain ies in ime es ima es and o e es ima ions o he di e gence imes o ecen axa [28,29]. Sho e di e gence imes would allow an al e na i e scena io o a small he d wi h a high equency o T1 eaching A ica, expanding and only hen spli ing in o he di e en T1 sub-haplog oups. Di e si y 2014, 6 181 Figu e 1. Dis ibu ions o majo au ine and indicine haplog oups. T1* indica es T1c1a1 [11], p e iously deno ed as AA [8]. Di e si y 2014, 6 182 Figu e 2. Mi ochond ial DNA (M DNA) haplog oup dis ibu ions in Eu opean and Sou hwes -Asian ancien DNA samples om domes ic ca le. Da a a e om [16–23]. Mig a ion om Cen al o Eas Asia led o he expansion o haplog oup T4. This is a sub a ian o T3, which is no obse ed in he wes , bu has been ound in Eas -Chinese ancien DNA da ing o 4500 BP [30], in mode n Ko ean bee ca le [10] and in mo e han hal o he Japanese ca le [31]. I is also a a equency o 21% in he No h-Sibe ian Yaku [32], indica ing a link be ween he Yaku and ca le om Eas -China. A simila expansion occu ed du ing he coloniza ion o he New Wo ld since he end o he 15 h cen u y. Haplog oup dis ibu ions, wi h T3 as majo and T1 as mino , e lec he Ibe ian ances y o Ame ican ca le. Al hough he T1 haplo ype T1c1a1 is spo adic in he Old Wo ld i eaches equencies o 31% in he Ca ibbean Lesse An illes islands and e en 50% in B azilian C iollo ca le [8,14,33]. Po uguese colonis s impo ed he i s ca le o B azil in 1534 om Cabo Ve de nea he Wes -A ican coas [34], while he English and F ench colonis s se led only in he 17 h cen u y in he Lesse An illes. This sugges s a scena io in which ca le ca ying he T1c1a1 haplo ype o igina ed ei he om Po ugal o A ica, g ew in numbe on Cabo Ve de o in B azil and we e la e expo ed o he nea by Ca ibbean isles. Indicine ma e nal lineages om haplog oups I1 and I2 di used om Sou h Asia o Sou hwes and Cen al Asia [9,35]. Haplog oups I1 p edomina ed in he ca le ha mo ed eas wa ds o Sou heas Asia and China. Popula ions wi h a mixed au ine and indicine ma e nal o igin a e ound in Sou hwes Asia, he Indus Valley, Cen al Asia, Nepal, Bhu an, China, Mongolian and B azil. The gayal popula ion om Yunnan in Sou h China combines I1 and T3 m DNA wi h pa e nal lineages om he gayal (Bos on alis) o wild gau (Bos gau us) [36]. In Indonesia, zebu in og essed in o local popula ions o domes ic Di e si y 2014, 6 183 ban eng (Bos ja anicus), which ha e pa ially e ained hei o iginal ja acine o igin in hei m DNA [37]. Ma e nal yak (Bos g unniens) in og ession has been obse ed in Nepal [38] and Qinghai [39]. Geog aphic di e en ia ion o ca le m DNA is clea ly s onge han obse ed o sheep, goa and ho se, which exhibi s a b oade dis ibu ion o he majo m DNA haplog oups [1]. Sequencing o ancien m DNA om emains o domes ic ca le ound in Eu ope, I an, China and he Ca ibbean in a iably shows con inui y wi h p esen -day animals om he same egion. This sugges s ha ab up shi s in haplo ype equencies we e caused by s ong ounde e ec s du ing he ea lies mig a ions o ca le, which appa en ly in ol ed only a ew indi iduals. I is plausible ha i was easie o anspo la ge g oups o he smalle and mo e manageable goa s and sheep, while mobili y o ho ses was p omo ed by ading and wa s. The s ong geog aphic di e en ia ion o m DNA in he Chinese popula ion o swamp ype o wa e bu alo [40] suppo s he hypo hesis ha di e en ia ion o ma e nal lineages co ela es wi h a low mobili y o he he ds. Selec ion o e s an al e na i e explana ion o he s ong phylogeog aphy seen in bo ine m DNA. Pu i ying selec ion ac ing on m DNA has been demons a ed o bo h bo ine and o he mammals [41], al hough i may be weake o domes ic li es ock han o wild species [42]. Posi i e selec ion may imp o e he adap a ion o ca le o di e en en i onmen s. One o he T4-speci ic subs i u ions leads o an L380M mu a ion in he cy och ome b gene and he G1324A subs i u ion in T1c1a1 causes a mu a ed RNA. Howe e , no di e ences ha e been ound in p oduc ion and ep oduc ion ai s be ween B azilian Guze a zebus ca ying au ine m DNA and hose ca ying indicine m DNA [43]. None heless, he e is no a p io i eason why m DNA-encoded gene p oduc s canno be in ol ed in selec ion and con ibu e o ai s ele an o adap a ion o p oduc ion, hus leading o geog aphic di e en ia ion o m DNA. 4. Conclusions We conclude ha he me a-analysis o bo ine m DNA sequences om bo h p esen and a chaeological samples allows o a global pic u e o geog aphic di e en ia ion o he ma e nal lineages, which ha e been shaped by popula ion bo lenecks du ing he wo ldwide dispe sal o ca le. As shown o haplog oup T1 in A ica [11,44], whole-m DNA sequencing may de ec addi ional sub-haplog oups in o ma i e o mo emen s o ca le be ween o wi hin con inen s and expansion o popula ions. Ancien DNA s udies con ibu e essen ially o he his o ic econs uc ions by p o iding geog aphic and his o ic ancho poin s o speci ic haplo ypes. Supplemen a y Ma e ials Supplemen a y ma e ials can be accessed a : h p://www.mdpi.com/1424-2818/6/1/178/s1. Acknowledgemen s We acknowledge se e al published o unpublished con ibu ions o he mi ochond ial DNA sequence da ase desc ibed in his epo . We app ecia e he sugges ions o bo h e iewe s. Di e si y 2014, 6 184 Au ho Con ibu ions Johannes A. Lens a ini ia ed his s udy and w o e he i s d a . Paolo Ajmone-Ma san, Albano Beja-Pe ei a, Ru h Bollongino, Daniel G. B adley, Licia Colli, Anna De Gae ano, Cei idwen J. Edwa ds, Luca Fe e i, Ca a ina Ginja, Pe e H is o , Juha Kan anen, Juan Ped o Li ón, Da id A. Magee, Ricca do Neg ini and Geo gi A. Radosla o con ibu ed o da a compila ion, Paolo Ajmone-Ma san, Luca Fe e i and Ma leen Felius o he his o ic in e p e a ion and Cei idwen J. Edwa ds o inal edi ing. Con lic s o in e es The au ho s decla e no con lic o in e es Re e ences 1. G oene eld, L.F.; Lens a, J.A.; Eding, H.; To o, M.A.; Sche , B.; Pilling, D.; Neg ini, R.; Finlay, E.K.; Jianlin, H.; G oene eld, E.; e al. Gene ic di e si y in a m animals: A e iew. Anim. Gene . 2010, 41, 6–31. 2. Lens a, J.A.; G oene eld, L.F.; Eding, H.; Kan anen, J.; Williams, J.L.; Tabe le , P.; Nicolazzi, E.L.; Sölkne , J.; Simiane , H.; Ciani, E.; e al. Molecula ools and analy ical app oaches o he cha ac e iza ion o a m animal di e si y. Anim. Gene . 2012, 43, 483–502. 3. Zede , M.A.; Emshwille , E.; Smi h, B.D.; B adley, D.G. Documen ing domes ica ion: The in e sec ion o gene ics and a chaeology. T ends Gene . 2006, 22, 139–155. 4. B adley, D.G.; Lo us, R.T.; Cunningham, C.; MacHugh, D.E. Gene ics and domes ic ca le o igin. E ol. An h opol. 1998, 6, 79–86. 5. Ajmone-Ma san, P.; Ga cia, J.F.; Lens a, J.A. On he o igin o ca le: How au ochs became ca le and colonized he wo ld. E ol. An h opol. 2010, 19, 148–157. 6. T oy, C.S.; MacHugh, D.E.; Bailey, J.F.; Magee, D.A.; Lo us, R.T.; Cunningham, P.; Chambe lain, A.T.; Sykes, B.C.; B adley, D.G. Gene ic e idence o Nea -Eas e n o igins o Eu opean ca le. Na u e 2001, 410, 1088–1091. 7. Mannen, H.; Kohno, M.; Naga a, Y.; Tsuji, S.; B adley, D.G.; Yeo, J.S.; Nyamsamba, D.; Zagdsu en, Y.; Yokohama, M.; Nomu a, K.; e al. Independen mi ochond ial o igin and his o ical gene ic di e en ia ion in No h Eas e n Asian ca le. Molec. Phylogene . E ol. 2004, 32, 539–544. 8. Ginja, C.; Penedo, M.C.; Melucci, L.; Qui oz, J.; Ma inez Lopez, O.R.; Re ida i, M.A.; Ma inez-Ma inez, A.; Delgado, J.V.; Gama, L.T. O igins and gene ic di e si y o New Wo ld C eole ca le: In e ences om mi ochond ial and Y ch omosome polymo phisms. Anim. Gene . 2010, 41, 128–141. 9. Chen, S.; Lin, B.Z.; Baig, M.; Mi a, B.; Lopes, R.J.; San os, A.M.; Magee, D.A.; Aze edo, M.; Ta oso, P.; Sasazaki, S.; e al. Zebu ca le a e an exclusi e legacy o he Sou h Asia Neoli hic. Molec. Biol. E ol. 2010, 27, 1–6. 10. Achilli, A.; Oli ie i, A.; Pellecchia, M.; Uboldi, C.; Colli, L.; Al-Zahe y, N.; Acce u o, M.; Pala, M.; Hooshia Kashani, B.; Pe ego, U.A.; e al. Mi ochond ial genomes o ex inc au ochs su i e in domes ic ca le. Cu . Biol. 2008, 18, R157–R158. Di e si y 2014, 6 185 11. Bon iglio, S.; Ginja, C.; de Gae ano, A.; Achilli, A.; Oli ie i, A.; Colli, L.; Tes aye, K.; Agha, S.H.; Gama, L.T.; Ca ona o, F.; e al. O igin and sp ead o Bos au us: New clues om mi ochond ial genomes belonging o haplog oup T1. PLoS One 2012, 7, e38601. 12. Achilli, A.; Bon iglio, S.; Oli ie i, A.; Malusa, A.; Pala, M.; Hooshia Kashani, B.; Pe ego, U.A.; Ajmone-Ma san, P.; Lio a, L.; Semino, O.; e al. The mul i ace ed o igin o au ine ca le e lec ed by he mi ochond ial genome. PLoS One 2009, 4, e5753. 13. S ock, F.; Edwa ds, C.J.; Bollongino, R.; Finlay, E.K.; Bu ge , J.; B adley, D.G. Cy och ome b sequences o ancien ca le and wild ox suppo phylogene ic complexi y in he ancien and mode n bo ine popula ions. Anim. Gene . 2009, 40, 694–700. 14. Bon iglio, S.; Achilli, A.; Oli ie i, A.; Neg ini, R.; Colli, L.; Lio a, L.; Ajmone-Ma san, P.; To oni, A.; Fe e i, L. The enigma ic o igin o bo ine m DNA haplog oup R: Spo adic in e b eeding o an independen e en o Bos p imigenius domes ica ion in I aly? PLoS One 2010, 5, e15760. 15. Bollongino, R.; Bu ge , J.; Powell, A.; Mashkou , M.; Vigne, J.D.; Thomas, M.G. Mode n au ine ca le descended om small numbe o Nea -Eas e n ounde s. Molec. Biol. E ol. 2012, 29, 2101–2104. 16. Bailey, J.F.; Richa ds, M.B.; Macaulay, V.A.; Colson, I.B.; James, I.T.; B adley, D.G.; Hedges, R.E.; Sykes, B.C. Ancien DNA sugges s a ecen expansion o Eu opean ca le om a di e se wild p ogeni o species. P oc. Royal Soc. B: Biol. Sci. 1996, 263, 1467–1473. 17. MacHugh, D.E.; T oy, C.S.; McCo mick, F.; Olsake , I.; Ey ho sdo i , E.; B adley, D.G. Ea ly medie al ca le emains om a Scandina ian se lemen in Dublin: Gene ic analysis and compa ison wi h ex an b eeds. P oc. Royal Soc. B: Biol. Sci. 1999, 354, 99–109. 18. Edwa ds, C.J.; MacHugh, D.E.; Dobney, K.M.; Ma in, L.; Russell, N.; Ho wi z, L.K.; McIn osh, S.K.; MacDonald, K.C.; Helme , D.; T esse , A.; e al. Ancien DNA analysis o 101 ca le emains: Limi s and p ospec s. J. A chaeol. Sci. 2004, 31, 695–710. 19. Ande ung, C.; Bouwman, A.; Pe sson, P.; Ca e e o, J.M.; O ega, A.I.; Elbu g, R.; Smi h, C.; A suaga, J.L.; Elleg en, H.; Go he s om, A. P ehis o ic con ac s o e he S ai s o Gib al a indica ed by gene ic analysis o Ibe ian B onze Age ca le. P oc. Na . Acad. Sci. USA 2005, 102, 8431–8435. 20. Kühn, R.; Lud , C.; Manha , H.; Pe e s, J.; Neumai , E.; Ro mann, O. Close gene ic ela ionship o ea ly Neoli hic ca le om Ziegelbe g (F eising, Ge many) wi h mode n b eeds. J. Anim. B eeding Gene . 2005, 122, 36–44. 21. Bollongino, R.; Edwa ds, C.J.; Al , K.W.; Bu ge , J.; B adley, D.G. Ea ly his o y o Eu opean domes ic ca le as e ealed by ancien DNA. Biol. Le . 2006, 2, 155–159. 22. Edwa ds, C.J.; Bollongino, R.; Scheu, A.; Chambe lain, A.; T esse , A.; Vigne, J.D.; Bai d, J.F.; La son, G.; Ho, S.Y.; Heupink, T.H.; e al. Mi ochond ial DNA analysis shows a Nea Eas e n Neoli hic o igin o domes ic ca le and no indica ion o domes ica ion o Eu opean au ochs. P oc. Royal Soc. B: Biol. Sci. 2007, 274, 1377–1385. 23. Scheu, A.; Ha z, S.; Schmölcke, U.; T esse , A.; Bu ge , J.; Bollongino, R. Ancien DNA p o ides no e idence o independen domes ica ion o ca le in Mesoli hic Rosenho , No he n Ge many. J. A chaeol. Sci. 2008, 35, 1257–1264. Di e si y 2014, 6 186 24. Cymb on, T.; F eeman, A.; Malhei o, M.I.; Vigne, J.D.; B adley, D. Mic osa elli e di e si y sugges s di e en his o ies o Medi e anean and No he n Eu opean ca le popula ions. P oc. Royal Soc. B: Biol. Sci. 2005, 272, 1837–1843. 25. Beja-Pe ei a, A.; Ca amelli, D.; Lalueza-Fox, C.; Ve nesi, C.; Fe and, N.; Casoli, A.; Goyache, F.; Royo, L.J.; Con i, S.; La i, M.; e al. The o igin o Eu opean ca le: E idence om mode n and ancien DNA. P oc. Na . Acad. Sci. USA 2006, 103, 8113–8118. 26. Pellecchia, M.; Neg ini, R.; Colli, L.; Pa ini, M.; Milanesi, E.; Achilli, A.; Be o elle, G.; Ca alli-S o za, L.L.; Piazza, A.; To oni, A.; e al. The mys e y o E uscan o igins: No el clues om Bos au us mi ochond ial DNA. P oc. Royal Soc. B: Biol. Sci. 2007, 274, 1175–1179. 27. K on, H. Roman li es ock a ming in sou he n I aly: The case agains en i onmen al de e minism. In Espaces In eg és e Ressou ces Na u elles dans l'Empi e Romain; Cla el-Lé êque, M., He mon, E., Eds.; P esses Uni e si ai es de F anche-Com é: Besançon, F ance, 2004; pp. 119–134. 28. Ho, S.Y.; La son, G.; Edwa ds, C.J.; Heupink, T.H.; Lakin, K.E.; Holland, P.W.; Shapi o, B. Co ela ing Bayesian da e es ima es wi h clima ic e en s and domes ica ion using a bo ine case s udy. Biol. Le . 2008, 4, 370–374. 29. Soub ie , J.; S eel, M.; Lee, M.S.; de Sa kissian, C.; Guindon, S.; Ho, S.Y.; Coope , A. The in luence o a e he e ogenei y among si es on he ime dependence o molecula a es. Molec. Biol. E ol. 2012, 29, 3345–3358. 30. Cai, D.; Sun, Y.; Tang, Z.; Hud, S.; Li, W.; Zhao, X.; Xiang, H.; Zhou, H. The o igins o Chinese domes ic ca le as e ealed by ancien DNA analysis. J. A chaeol. Sci. 2014, 41, 423–434. 31. Mannen, H.; Kojima, T.; Oyama, K.; Mukai, F.; Ishida, T.; Tsuji, S. E ec o mi ochond ial DNA a ia ion on ca cass ai s o Japanese Black ca le. J. Anim. Sci. 1998, 76, 36–41. 32. Kan anen, J.; Edwa ds, C.J.; B adley, D.G.; Viinalass, H.; Thessle , S.; I ano a, Z.; Kiselyo a, T.; Cinkulo , M.; Popo , R.; S ojano ic, S.; e al. Ma e nal and pa e nal genealogy o Eu asian au ine ca le (Bos au us). He edi y 2009, 103, 404–415. 33. Magee, D.A.; Meghen, C.; Ha ison, S.; T oy, C.S.; Cymb on, T.; Gailla d, C.; Mo ow, A.; Mailla d, J.C.; B adley, D.G. A pa ial A ican ances y o he C eole ca le popula ion o he Ca ibean. J. He ed. 2002, 93, 429–432. 34. Bo ges Lopes, M.A.; Ma quez de Rezende, E.M. ABCZ His ó ia e His ó ias; Câma a B asilei a do Li o: Sao Paulo, B azil, 2001. (In Po uguese) 35. Magee, D.A.; Mannen, H.; B adley, D.G. Duali y in Bos indicus m DNA di e si y: suppo o geog aphical complexi y in zebu domes ica ion. In The E olu ion and His o y o Human Popula ions in Sou h Asia; Pe aglia, M.D., Allchin, B., Eds.; Sp inge : New Yo k, NY, USA, 2007; pp. 385–391. 36. Gou, X.; Wang, Y.; Yang, S.; Deng, W.; Mao, H. Gene ic di e si y and o igin o Gayal and ca le in Yunnan e ealed by m DNA con ol egion and SRY gene sequence a ia ion. J. Anim. B eeding Gene . 2010, 127, 154–160. 37. Mohamad, K.; Olsson, M.; an Tol, H.T.; Mikko, S.; Vlamings, B.H.; Ande sson, G.; Rod iguez-Ma inez, H.; Pu wan a a, B.; Paling, R.W.; Colenb ande , B.; e al. On he o igin o Indonesian ca le. PLoS One 2009, 4, e5490.