You are on page 1of 10

Nature Reviews Genetics 4, 900-910 (2003); doi:10.



Michael W. Bruford1, Daniel G. Bradley2 & Gordon Luikart3

1 ( 3

about the author

Cardiff School of Biosciences, Main Building, Cathay Park, P Bo! 915, Cardiff C"1# 3$%, &K' )e*art+ent of ,enetics, S+urfit -nstitute, $rinity College, )u.lin (, -reland' %a.oratoire d/0cologie 1l*ine, ,2no+i3ue des Po*ulations et Biodi4ersit2, ((33 5ue de la Piscine, B'P' 53 Centre 6ational 5echerche Scientifi3ue, &M5 5553, &ni4ersit2 7ose*h "ourier, "839#:1 ,reno.le, Cede! 9, "rance'

!orre "o#$e#!e to% Michael ;' Bruford BrufordM;<cardiff'ac'uk

A er&e o' re!e#t (e#et&! tu$&e ha re)ea*e$ the re+ar,ab*- !o+"*e. "&!ture o' $o+e t&!at&o# &# both Ne/ 0or*$ a#$ O*$ 0or*$ *&)e to!,1 2- !o+"ar&#( +&to!ho#$r&a* a#$ #u!*ear DNA e3ue#!e o' +o$er# bree$ /&th the&r "ote#t&a* /&*$ a#$ $o+e t&! a#!e tor 4 /e ha)e (a&#e$ #e/ &# &(ht &#to the t&+&#( a#$ *o!at&o# o' $o+e t&!at&o# e)e#t that "ro$u!e$ the 'ar+ a#&+a* o' to$a-1 The rea* ur"r& e ha bee# the h&(h #u+ber o' $o+e t&!at&o# e)e#t a#$ the $&)er e *o!at&o# &# /h&!h the- too, "*a!e 5 'a!tor /h&!h !ou*$ ra$&!a**- !ha#(e our a""roa!h to !o# er)&#( *&)e to!, b&o$&)er &t- re our!e &# the 'uture1 )etailing the e4olutionary and de+ogra*hic history of hu+ans, and of the ani+als and *lants that =e ha4e ) M0S$-C1$0), has traditionally .een the real+ of e4olutionary 16$>5 P % ,-S$S and 15C>10 B- % ,-S$S' 5ecently, ho=e4er, the use of +olecular genetics has .egun to ha4e a +a?or i+*act on our understanding of ho= these e4ents took *lace' S*ecifically, recent studies ha4e allo=ed the identification of the =ild ancestors of +odern li4estock and the nature of li4estock e!*ansion in *ast +illennia 1, (' -nfor+ation of this ty*e is interesting as it tells us a great deal a.out oursel4es, es*ecially our history and the =ay in =hich =e ha4e sha*ed such e!traordinary .iological di4ersity in a relati4ely short *eriod of ti+e' "urther+ore, co+.ining e4olutionary studies of hu+ans 3, do+estic ani+als:, 5 and cro*s1 can gi4e us a uni3ue *ers*ecti4e on hu+an societies throughout the =orld' $hese data *otentially ha4e +ore i++ediate i+*ortance for the +anage+ent and conser4ation of today/s ani+al and *lant genetic resources' $he loss of agricultural di4ersity in the face of increasing *ressures fro+ +odern far+ing is a cause for concern' "irst, +uch of the di4ersity that is .eing lost is unkno=n, including large nu+.ers of =hole li4estock .reeds, and second, di4ersity that is undocu+ented at *resent @for e!a+*le, that =hich can .e found in locally ada*ted *o*ulationsA +ight contain genetic +aterial of 4alue for future *roduction' $he seriousness of the situation has *ro+*ted the "ood and 1griculture rganiBation of the &nited 6ations to initiate an e!ercise to docu+ent the state of the ;orld/s 16-M1% ,060$-C 50S &5C0S @1n,5A C a *rocess that =ill co+*le+ent the sa+e e!ercise for *lants, =hich =as co+*leted 1# years agoD' Such an e!ercise needs to dra= on as +uch rele4ant data as *ossi.le, including the +olecular di4ersity of the ;orld/s 1n,5, =hich has .een identified as i+*ortant' )ata fro+ +olecular studies of li4estock do+estication can therefore .e used to assist in the conser4ation of the .e=ildering di4ersity of li4estock 1n,5' -n this re4ie=, =e sho= ho= genetic studies can enhance our understanding of do+estication, .y allo=ing the identification of =ild ancestors and the location and ti+ing of do+estication e4ents' -n addition, =e discuss ho= the genetic di4ersity of +odern li4estock can .e assessed on different geogra*hic scales, and ho= *atterns of di4ersity 4ary a+ong s*ecies' ;e focus on the large +eat8 and +ilk8*roducing and *ack +a++alsE cattle, horses, shee*, *igs, goats, .uffalo and C1M0%-)S' ,round.reaking =ork has also .een carried out on do+estic carni4ores :, fo=l5 and fishF, and has shed light on different +odes of ani+al do+estication that are .eyond the sco*e of this re4ie=' >o=e4er, it is interesting to note that do+estic dog:, chicken and co++on car*F studies i+*licate an east 1sian centre of do+estication, =hich is a *attern that is re*eated in se4eral of the li4estock studies descri.ed here' Do+e t&!at&o# a#$ (e#et&! tru!ture >y*otheses a.out =here and =hen li4estock do+estication took *lace ha4e .een generated fro+ nu+erous 15C>10 G % ,-C1% studies @see .elo=A' Most li4estock do+estication e4ents are thought to ha4e occurred at around the sa+e ti+e in south=est 1sia, east 1sia and the 1+ericas, 9,###H1#,### years .efore *resent @

IBPA, and it is *ossi.le that this con?unction =as not .y chance'

1t that ti+e, the cli+ate, =hich fro+ 19,### had started to .eco+e =ar+er and +ore seasonal, fa4oured *lants =ith large roots and tu.ers and large seeded annual *lants' Such s*ecies are easy to har4est, culti4ate and store and so are =ell suited to far+ing' $hese s*ecies * .eca+e increasingly i+*ortant food resources during seasons in =hich food =as una4aila.le' ;ith the cli+atic re4ersal of the Iounger )ryas cold *eriod @1(,(##H11,1## A, the de+and for culti4ated and stora.le food increased and led to the do+estication of s*ecies such as rice, =heat and legu+es1, 9' 1s the cli+ate =ar+ed, so+e hu+an *o*ulations started e!*anding ra*idly and *o*ulation centres .eca+e esta.lished in regionally i+*ortant sites' Settle+ents tended to .e located in naturally fertile areas that =ere suita.le for agriculture, or in locations that linked different land+asses, and so =ere natural sto**ing8off *oints for +igrating *eo*les 1' $he indigenous *o*ulation, together =ith +igratory *o*ulations, needed to .e su**lied =ith food9, and this =ould ha4e *ro4ided another sti+ulus for far+ing and the do+estication of agricultural s*ecies' ;hether the sa+e *ressures led to the esta.lish+ent of agriculture in different foci is still a +atter of de.ate 1#81(' $he three *rinci*al areas of li4estock do+estication are generally acce*ted as south=est 1sia @the "05$-%0 C50SC06$ and its eastern +argin, to=ards the -ndus 4alley region1A and east 1sia @China and countries south of ChinaA and the 1ndean chain of South 1+erica @"ig' 1A' Cattle, shee*, goats, *igs and .uffalo =ere do+esticated in t=o 1sian regions, =hereas lla+as and al*acas =ere do+esticated in South 1+erica' $he horse is a nota.le e!ce*tion' -t is thought to ha4e .een do+esticated on nu+erous inde*endent occasions in +ore northerly latitudes 13, 1:' -n addition, the horse is a**arently the +ost recently do+esticated +a?or li4estock s*ecies @ D,###






"igure 1 J The "r&#!&"a* !e#tre o' a#&+a* $o+e t&!at&o#1

$he *utati4e sites =here ancestral *o*ulations of +odern li4estock =ere do+esticated C the northern 1ndean chain, south=est 1sia @including the -ndus 4alleyA and east 1sia, res*ecti4ely' -t should .e noted that the +a* does not include horses, =hich =ere a**arently do+esticated +any ti+es in +ore northerly latitudes'

$he transition of hu+ans fro+ hunting, to the ta+ing of =ild ani+als .y ani+al hus.andry, to e4entual do+estication is an e!tre+ely acti4e area of research for archaeoBoologists' $here is considera.le de.ate concerning the a.ility of *resent archaeoBoological studies to detect the occurrence and ti+ing of these transitions, as =ell as to identify changes in the age and se! structure of do+esticated *o*ulations 15819' $his lea4es o*en the 3uestion of =hich *o*ulations, su.s*ecies or e4en s*ecies of =ild ancestors =ere do+esticated and to =hat degree they ha4e contri.uted to the gene *ool of +odern8day do+estic li4estock' Molecular studies allo= these 3uestions to .e ans=ered' )618.ased +arkers, =hich can .e a**lied to *hylogenetics, *o*ulation di4ersity and the genetic identification of indi4iduals, ha4e .een de4elo*ing since the 19F#s 19, (# .ut ha4e only .een acti4ely a**lied to studies of ani+al do+estication and di4ersity since the early 199#s (1, ((' Choo &#( +o*e!u*ar +ar,er $o hel* understand the origins of do+estication of a li4estock s*ecies, an ideal +olecular +arker should ha4e se4eral characteristics' "irst, it should .e sufficiently e4olutionarily conser4ed to allo= the identification of the =ild ta!on or *o*ulation fro+ =hich the s*ecies descends' Second, the +arker should .e 4aria.le and structured enough across the geogra*hical range of the s*ecies so that the a**ro!i+ate locality of do+estication can .e identified' $hird, the +arker should e4ol4e at a ra*id .ut constant rate C this feature allo=s the origin of a *articular *oly+or*his+ to .e dated' $his co+.ination of characteristics is difficult to find, .ut fortunately, in ani+al e4olutionary studies, there is such a +arkerE +itochondrial @+tA )61' 1t *resent, +t)61 is .y far the +ost =idely used +olecular tool in do+estication studies' +t)61 is a s+all *las+id C less than (# k. in +ost +a++als C that is located only in the +itochondrial organelle' -t is highly 4aria.le =ithin s*ecies, such that in hu+ans for ?ust one highly 4aria.le section of +t)61 C the control region C o4er 5## distinct >1P% $IP0S ha4e .een identified(3' 1 recent study of the control8region di4ersity in do+estic goats @Capra hircusA identified 331 ha*loty*es fro+ :#D indi4iduals (:' +t)61 and *articularly the control8region se3uence @Bo! 1A e4ol4es e!tre+ely ra*idly co+*ared =ith nuclear )61, and is conse3uently a *o=erful tool for esta.lishing the le4els of genetic di4ersity and *hylogenetic structure =ithin a s*ecies' +t)61 can also tell us a.out the recent de+ogra*hic *rocesses affecting a *o*ulation, for e!a+*le =hether a *o*ulation has undergone a recent de+ogra*hic e!*ansion, or has a +ore co+*le! history @Bo! 1A' Ma++alian +t)61 is also al+ost e!clusi4ely +aternally inherited, is effecti4ely ha*loid and does not undergo reco+.ination' $hese characteristics +ean that each indi4idual has a single ha*loty*e and that *hylogenetic analyses are relati4ely straightfor=ard to inter*ret' -ndeed, .ecause of these features +t)61 has .een the *redo+inant +olecule used to deter+ine 4erte.rate *hylogeny for the *ast (# years(5' 1lthough +t)61 analysis can .e e!tre+ely infor+ati4e in do+estication studies @.oth =ithin and a+ong s*eciesA, its uses are li+ited' -t can .e a *oor *redictor of o4erall geno+ic di4ersity, .ecause it .eha4es like a single locus and is an e!tra8nuclear genetic +arker =ith s*ecific e4olutionary dyna+ics' Crucially, as it is +aternally inherited, +t)61 does not detect +ale8+ediated gene flo=, =hich has had a *o=erful influence on the e4olution of li4estock s*ecies in +odern ti+es(D' -t is useful to consider ho= +t)61 di4ersity is /ca*tured/ during do+estication, as the segregation of an +t)61 lineage =ithin a li4estock *o*ulation can only ha4e occurred through the do+estication of a =ild fe+ale or through the incor*oration of a fe+ale into an e!isting do+estic stock (' 1lternati4e genetic +arkers include 4aria.le se3uences on the I chro+oso+e' >o=e4er, this chro+oso+e is +uch less 4aria.le =ithin s*ecies than +ost other geno+ic se3uences, =hich +akes difficult its routine use for *hylogenetic analyses' 1nalysis of the I chro+oso+e also lacks the *o=er of +ulti*le8.and *rofile +arkers, such as 1MP%-"-0) "51,M06$ %06,$> P %IM 5P>-SMS @1"%PsA, (F =hich assay 4ariation at +any loci si+ultaneously' 1 disad4antage of 1"%P +arkers is that they sho= a do+inant +ode of inheritance, .ecause only one allele is detected *er locus' $his can reduce the *o=er of *o*ulation genetic analyses, =hich generally re3uire +ore infor+ati4e codo+inant +arkers' 6e4ertheless, 1"%P *rofiles are highly infor+ati4e as they *roduce +any *oly+or*hic +arkers and are therefore .eing increasingly used in *lant and ani+al do+estication studies1, (9' $he other +ain class of +olecular +arkers that are used in do+estication studies are +icrosatellites (9' $hese +arkers are short re*etiti4e ele+ents in geno+ic )61, such as *oly8dinucleotide re*eats @for e!a+*le, 1C1C1C'''A, that are codo+inantly inherited' $he of re*eats 4aries .et=een alleles and there are +any thousands of +icrosatellite loci throughout li4estock geno+es' -ndeed, +icrosatellites ha4e for+ed the .asis of +ost of the +ore recent li4estock genetic +a*s, and they =ere 3uickly found to .e useful in characteriBing di4ersity =ithin li4estock *o*ulations and .reeds((' Microsatellites ha4e three *ri+ary uses in do+estication studies' "irst, they can .e used to 3uantify genetic 4ariation =ithin and a+ong li4estock *o*ulations or .reeds3#' Second, they allo= the docu+entation of ad+i!ture @genetic +i!ingA a+ong li4estock *o*ulations (D, 31' $hird, +icrosatellite data can .e used to assign indi4iduals to genetically si+ilar grou*s at the *o*ulation, .reed or s*ecies le4els 3(83:' Microsatellites +arkers are also highly sensiti4e to genetic B $$%060CKS and selection35, .oth of =hich are likely to ha4e occurred during do+estication e4ents @see section on future directionsA' 1n e!a+*le of ho= +icrosatellites can .e highly discri+inatory =hen co+*aring alternati4e =ild s*ecies as the genetic ancestors of +odern li4estock31 is sho=n in Bo! (' 6e#et&! a#a*- & o' $o+e t&!at&o# $he use of genetic +arkers has re4ealed an e!traordinary a+ount of 4ariation and co+*le!ity in the do+estication of li4estock, in ter+s of the nu+.ers and ty*es of *rogenitors that contri.uted genetic +aterial during do+estication, and the of occasions that si+ilar stocks =ere do+esticated' Livestock progenitors. -n the 1+erican arena of ani+al do+estication, attention has so far focused on the South 1+erican ca+elids 31, 3D and =hether the +odern8day al*aca @Vicugna pacos A and lla+a @Lama glamaA descended fro+ either the =ild guanaco @Lama guanicoeA or 4icuKa @Vicugna vicugna A' +t)61 analysis has sho=n that the lla+a and al*aca ha4e ha*loty*es that originate fro+ .oth =ild s*ecies, .ut that +ost of

the indi4iduals ty*ed ha4e guanaco8ty*e +t)61, =hich indicates that there is a guanaco ancestry for .oth do+estic for+s' Su.se3uent +icrosatellite analysis sho=ed that this =as a +isleading *icture that =as *ri+arily the result of hy.ridiBation .et=een +ale al*aca and fe+ale lla+a31 @Bo! (A' >o=e4er further +t)61 analysis is re3uired to elucidate the of do+estication e4ents that ha4e contri.uted to the +odern8day lla+a and al*aca' Both of these li4estock s*ecies are thought to ha4e originated in the high 1ndes around 9,###




Perha*s the first indication that li4estock do+estication =as a +ore co+*le! *rocess than so+e authors .elie4ed ca+e fro+ +itochondrial studies of cattle(1, 39' $here are t=o *rinci*al distinct cattle ty*es found today, Be.u and taurine' Ge.u cattle ha4e a shoulder hu+* and are found +ainly in eastern 0urasia and eastern 1frica' By contrast, the taurine cattle lack a hu+* and are the *redo+inant cattle of 0uro*e, north and =est 1frica and the Middle 0ast' So+e authors ha4e classified the t=o ty*es as se*arate s*eciesL Bos indicus @Be.uA, and Bos taurus @taurineA cattle' -nitially, ho=e4er, the =idely held 4ie= =as that .oth ty*es =ere +erely differentiated for+s that originated fro+ a single do+estication e4ent' Molecular +arkers =ere used to in4estigate the intriguing origins of these cattle' $aurine cattle fro+ 0uro*e and 1frica and Be.u cattle fro+ -ndia and 1frica =ere co+*ared at the +olecular le4el' Sur*risingly, -ndian Be.u cattle =ere found to ha4e *rofoundly different =hole +t)61 50S$5-C$- 6 "51,M06$ %06,$> P %IM 5P>-SM @5"%PA *rofiles39 and control8region se3uences 39 =hen co+*ared =ith .oth 0uro*ean and 1frican taurine cattle and 1frican Be.u cattle C =hich all shared si+ilar se3uences' $he le4el of se3uence di4ergence .et=een the t=o +t)61 lineages =as consistent =ith a +ost recent co++on ancestor dating to hundreds of thousands of years ' >o=e4er, cattle do+estication =as kno=n to ha4e occurred +uch later than this, =ithin the last 1#,### years :#' So, the +ost *ro.a.le e!*lanation for this high le4el of +olecular di4ergence =as that genetically differentiated su.s*ecies of the ancestral =ild cattle Bos primigenius @also kno=n as aurochsA had .een do+esticated in different regions of 0urasia(1' 04ents since these initial do+estications ha4e .een harder to disentangle using +t)61' "or e!a+*le, the data sho=ed that 1frican Be.u +ight only ha4e taurine +t)61(1, =hich see+ed curious as it =as thought that these Be.u cattle originally ca+e to 1frica fro+ 1sia and the Middle 0ast, trans*orted .y no+adic *astoralists' >o=e4er, later studies using +icrosatellites and I8chro+oso+e )61 sho=ed that the nuclear )61 of 1frican Be.u cattle =as +ost si+ilar to that found in other Be.u cattle *o*ulations' $he reason for this difference =as that +t)61 studies =ere not a.le to detect Be.u genes @*assed into the local taurine *o*ulation .y Be.u .ullsA, .ecause +ale +itochondrial )61 alleles are not trans+itted to descendent generations (D' -n li4estock .reeding selected +ales often ha4e +any offs*ring, =hereas fe+ales are li+ited to only a fe=' So it is easy to i+agine that the geno+es of 1frican Be.u cattle largely deri4e fro+ +ale originating fro+ 1sia and the Middle 0ast des*ite their +t)61 a**arently .eing deri4ed fro+ a fe= fe+ale taurine founders' Most recently, the origins of 0uro*ean taurine cattle ha4e .een illu+inated .y a large8scale study of the 4ariation in control8region +t)61 4ariation in :## cattle fro+ 0uro*e, 1frica and the 6ear 0ast' $he study also used ancient8)61 +ethods, =hich ha4e .een increasingly used to identify *hylogenetic affiliations fro+ the re+ains of organis+s ranging fro+ hu+ans to .acteria :1' Skeletal re+ains found in the &nited Kingdo+ fro+ four =ild aurochs =ere radiocar.on dated to 3,F(#HF,3(# and their *hylogenetic relationshi*s =ere deter+ined' Sur*risingly, they =ere found to .e unrelated to +odern8day &K do+estic cattle, =hich =ere instead +ore si+ilar to +odern cattle in the 6ear 0ast @"igs (,3A' $hese data indicate that at least the +aternal origins of 0uro*ean cattle are consistent =ith the s*read of cattle .y cattle far+ers fro+ the "ertile Crescent, and not local, inde*endent do+estication :('



"igure ( J Ph-*o(e#et&! !o+"*e.&t- &# +o$er#7$a- !att*e a#$ hor e 1

$he .ranch lengths are *ro*ortional to the a+ount of e4olutionary change that has occurred along the+' a J 1 re*resentation of the +itochondrial @+tA )61 tree *roduced for +odern8day hu+*ed @ Bos indicusA and =estern @Bos taurusA cattle and the ancient British aurochs @also kno=n as =ild cattleL Bos primigeniusA that is .ased on (#1 .ase *airs @.*A of control8region se3uence:(' 6ote the *hylogenetic distincti4eness of the aurochs co+*ared =ith +odern8 day 0uro*ean cattle, including .reeds fro+ the sa+e island' $he scale .ar re*resents #'#1 su.stitutions *er .*' Part a is +odified =ith *er+ission fro+ 5ef' :( M Mac+illan MagaBines %td @(##1A' b J 1 reduced +edian net=ork of the +ost P15S-M 6- &S connections a+ong D5( +itochondrial ha*loty*es fro+ the horse @ Equus caballusA that is .ased on (:F .* of control8region se3uence13' $he siBe of the yello= circles re*resents the of indi4iduals for =hich a ha*loty*e se3uence =as o.tained' $he orange circles re*resent *utati4e inter+ediate ha*loty*es that ha4e not yet .een found' $he codes used to la.el the +ost co++on ha*loty*es corres*ond to those used in 5ef' 53' $he dashed lines .et=een ha*loty*es re*resent unresol4ed e3ually *arsi+onious connections .et=een se3uences' Cluster 1 @green shaded areaA is found only in PrBe=alski/s horse @Equus caballus przewalskiA, =hich is a *ossi.le ancestral s*ecies for do+estic horses' So+e of the +ore co++on ha*loty*es sho= li+ited geogra*hical structure' "or e!a+*le, C1 and 0 are found *redo+inantly =ithin northern 0uro*ean *onies and )1 is +ost co++on in north 1frican and -.erian sa+*les' 4erall, the net=ork sho=s the co+*le! *attern of *hylogenetic relationshi*s a+ong +itochondrial ha*loty*es fro+ the horse' Part b is +odified =ith *er+ission fro+ 5ef' 13 M 6ational 1cade+y of Sciences, &S1 @(##(A' "igure 3 J Ph-*o(e#et&! !o+"*e.&t- &# +o$er#7$a- hee" a#$ (oat 1

$he .ranch lengths are *ro*ortional to the a+ount of e4olutionary change that has occurred along the+' a and b J 1 +itochondrial )61 M1N-M&M8%-K0%-> ) *hylogeny for shee* @Ovis ariesL using 1#:5 .ase *airs @.*A out of 1333 .* of control8region se3uenceA:D and a 60-,>B &587 -6-6, tree for goats @Capra hircusL using :91 .* of control8region se3uenceA(: and their *utati4e =ild ancestors indicating that there are t=o and three do+estic +itochondrial ha*logrou*s, res*ecti4ely' $he scale .ar in a re*resents #'#1( su.stitutions *er 4aria.le )61 site, =hich roughly corres*onds to 5##,### years of e4olution' -n *art b, the nu+.ers and letters that follo= the s*ecies na+es re*resent the different ha*logrou*s' $he nu+.ers on the .ranches re*resent the *ercentage of B $S$51P re*licates that su**ort that *articular .ranch' %ineage C 1%0SC06C0 ti+es are 5##,### years .efore *resent @ A and a**ro!i+ately (##,### , res*ecti4ely' $hese coalescence ti+es *redate do+estication .y +ore than an order of +agnitude' Part a is +odified =ith *er+ission fro+ 5ef' :D M $he 5oyal Society @(##(A' Part b is +odified =ith *er+ission fro+ 5ef' (: M 6ational 1cade+y of Sciences, &S1 @(##1A'



$he use of ancient )61 has also *ro4ed crucial in unra4elling dog do+estication, =here it see+s that the ld ;orld, *articularly east 1sia, =as an i+*ortant area:, :3' -n addition, analysis of +odern sa+*les and )61 fro+ historical re+ains has sho=n that do+estication of the horse @Equus caballus A =as also a co+*le! *rocess13, 1:, ::' $he +ost recent of these e3uine studies13 found that control8region se3uences grou* into 1F *hylogenetic lineages @"igs (,3A' So+e of the grou*s cluster =ith +odern horse .reeds or geogra*hic locations, .ut +any do not' $he authors esti+ated that at least FF +ares +ust ha4e .een do+esticated to gi4e rise to the +odern le4els of control8region di4ersity' $his study used conser4ati4e esti+ates of the +utation rate @1 *er 1##,### yearsA and assu+ed that do+estication first occurred 9,:## ' $he clear conclusion fro+ these studies is that horses +ust ha4e .een do+esticated nu+erous ti+es' "urther se3uence in4estigation +ight lead to a +ore ro.ust esti+ate of the of ti+es and *laces that =ere in4ol4ed in horse do+estication' +t)61 analysis has also re4ealed a co+*le! *attern of do+estication in goats(:, =ith at least three di4ergent lineages ca*tured during at least t=o hy*othesiBed do+estication e4ents in the 6ear 0ast and in 1sia' $=o control8region lineages ha4e also .een descri.ed in shee* @ Ovis ariesA:5,


, =hich correlate =ell, .ut not co+*letely, =ith +odern fat8 and thin8tailed *henoty*ic 4arieties @"igs (,3A, and indicate that at least t=o do+estication e4ents occurred in this s*ecies' >o=e4er, a lack of rele4ant +odern =ild shee* sa+*les has ha+*ered the +ore accurate *in*ointing of =here and =hen these e4ents took *lace' $=o di4ergent +t)61 lineages re*resenting s=a+* and =ater .uffalo @ Bubalus bubalis A ha4e also .een descri.ed, =hich indicates that there =ere inde*endent do+estication e4ents :F, :9' "inally, this intriguing e+erging *attern of 0astH;est duality in do+estication is co+*leted in *igs @Sus scrofa domesticus A, for =hich +t)61 e4idence has consistently su**orted at least t=o do+estication e4ents, one fro+ a 6ear 0astern or 0uro*ean =ild .oar s*ecies and one fro+ an 1sian s*ecies :9851'

-n su++ary, it see+s clear fro+ the di4ergent +t)61 lineages in all large do+esticated +eat8 and +ilk8*roducing li4estock, a*art fro+ the horse, that highly di4ergent *o*ulations or different s*ecies =ere in4ol4ed in these do+estication e4ents' $a.le 1 su++ariBes these data and =hat is kno=n at the +olecular le4el a.out the ancestors of +odern li4estock'

$a.le 1 J 6e#et&! $&)er &t- &# *&)e to!, a#$ the&r "ote#t&a* a#!e tor

$herefore, it see+s that shee*, goats, cattle, .uffalo and *igs under=ent at least t=o inde*endent do+estication e4ents in east 1sia, 0uro*e or the 6ear 0ast' -n +arked contrast, horses @and * dogsA ha4e a +ore co+*le! history that is characteriBed .y nu+erous do+estication e4ents =orld=ideL it =ill .e interesting to see ho= these a**arently si+*le and +ore co+*le! stories de4elo* =ith +ore data, es*ecially data that in4ol4es ancient )61' >o=e4er, ancient8)61 studies +ight *ro4e increasingly difficult .ecause at *resent identifying the *recise localiBation of do+estic e4ents is ha+*ered .y difficulties in a+*lifying )61 fro+ archaeological sites in =ar+er regions' -t is also a challenge to co+*rehensi4ely sa+*le e!tant =ild *o*ulations' nce these technical and logistical *ro.le+s are o4erco+e future studies should .e a.le to resol4e these issues' $he do+estication histories of se4eral 0urasian do+estic s*ecies C the yak @ Bos grunniensA, donkey @Equus asinusA and ca+el @Camelus bactrianus and Camelus dromedariesA C are as yet *oorly characteriBed .y +olecular +arkers' >o=e4er, these s*ecies are no= .eing studied, and it =ill .e e!tre+ely interesting to see =hether the *atterns that e+erge follo= the si+*le @for e!a+*le, single, local originA or co+*le! *atterns that ha4e .een found in the li4estock s*ecies already studied' 6e#et&! $&)er &t- to$aSo, =hat do these co+*le! *atterns of *ast do+estication i+*ly for +odern *atterns of genetic di4ersity across indi4iduals, .reeds, do+estic /s*ecies/ and geogra*hical BonesO S*ecies such as cattle and shee* =ere do+esticated in the 6ear 0ast and are no= under intense hus.andry in 0uro*e and other *arts of the =orld =here li4estock rearing is a +a?or industry' -n the a.sence of large8scale recurrent gene flo=, =e +ight e!*ect that +ost of the genetic di4ersity for these s*ecies =ould .e *resent in the 6ear 0ast =here they =ere first do+esticated' $his di4ersity is e!*ected to decline as the distance fro+ the do+estication centres increases .ecause the 6eolithic cattle far+ers res*onsi.le for originally trans*orting these li4estock =est=ards only took s+all sa+*les of the di4erse eastern stock' $his *attern is indeed seen in cattle and shee* :(, 5(, .ut it is not so e4ident in goats(:' 1nalysis of +olecular 4ariance @1M P1A finds that in goats only 1#Q of +t)61 4ariation is *artitioned a+ong continents @"ig' :A, as o**osed to R5#Q in cattle39 and 35Q in shee*5(' -nterestingly, this indicates that goats +ight ha4e .een +ore easily or +ore =idely trans*orted throughout historical ti+es than shee* or cattle, =hich is consistent =ith goats .eing e!tre+ely hardy and ada*ta.le (:'

"igure : J Catt*e a#$ (oat +&to!ho#$r&a* $&)er &t- &# Eura &a1

0ach *ie diagra+ re*resents the total sa+*led control8region ha*loty*es in a *articular area for either cattle @ Bos taurus and Bos indicusL on the leftA or goats @Capra hircusL on the rightA' 0ach s*ecific ha*loty*e is re*resented .y a different colour @see keyA' ,oats and cattle sho= contrasting *atterns of +itochondrial @+tA )61 control8region lineage di4ersity o4er their geogra*hic range in =estern 0urasia' Cattle sho= a .road decline in di4ersity fro+ east to =est, as *redicted fro+ a gradual loss of di4ersity co+*ared =ith their ancestral *o*ulation during the 6eolithic e!*ansion fro+ south=est 1sia to northern 0uro*e :(, D9' -nterestingly, the *rinci*al 1frican ha*loty*e @$1A occurs rarely in the 6ear 0ast, indicating that there is a +ore shar* di4ergence * o=ing to se*arate =ild origins @that is, $1 +ight originate fro+ north east 1fricaA' By contrast, goats sho= +uch less structure, =hich could .e attri.uted to their relati4e /*orta.ility/(, (: and the fact that they ha4e .een +uch +ore e!tensi4ely trans*orted across the glo.e' Modified =ith *er+ission fro+ 5ef' (: M 6ational 1cade+y of Sciences, &S1 @(##1A'

$he +olecular signature of ra*id de+ogra*hic e!*ansions that are associated =ith large8scale do+estication and diffusion across the glo.e can .e seen in the +t)61 +is+atch distri.utions @Bo! (A of these do+estic s*ecies(:, 5(' Most ne= se3uence 4ariants are the result of recent +utations and are relati4ely closely related =ithin different do+estic +itochondrial lineages' >o=e4er, in other *arts of the =orld the *atterns of genetic di4ersity =ill not necessarily .e the sa+e' -solated andSor recently esta.lished li4estock *o*ulations @for e!a+*le, those esta.lished at the ti+e of 0uro*ean coloniBationA ty*ically sho= +ore co+*le! genetic signatures o=ing to their unusual histories' $he i+*act of geogra*hy, trans*ortation and -6$5 ,50SS- 6 on genetic di4ersity can clearly .e seen in studies of cattle fro+ 1sia to South 1+erica53855' Most recently, co+*rehensi4e sur4eys of 1frican cattle using +t)61 and +icrosatellites su**ort the +odel that they +ight ha4e originated fro+ the local do+estication of 1frican =ild o!en' $hese ani+als =ere undou.tedly genetically si+ilar to those that ga4e rise to 0uro*ean and 6ear 0astern cattle, .ut ha4e left a genetic legacy that is sufficiently distinct to su**ort archaeology that indicates a 6orth 1frican do+estication :(, 5D'

$he o4erlaid *atterns of .oth 0uro*ean and 1sian cattle introgression are also clearly sho=n in *atterns of +icrosatellite allele fre3uency 4ariation5D C illustrating the *o=er of these +arkers to un*ack nu+erous ancestral influences, so+eti+es =hen +t)61 alone gi4es an inco+*lete *icture' -n shee*, the t=o +itochondrial lineages =ere first disco4ered in 6e= Gealand 5F, =hich indicates that +t)61 fro+ .oth do+estication e4ents ha4e found their =ay into the 6e= Gealand flock' Su.se3uent +t)61 studies in 0uro*ean shee* ha4e sho=n that +ore recent introgression has * occurred fro+ east to =est, as the eastern shee* +itochondrial lineage is no= found in a fe= =estern 0uro*ean .reeds, in +arked contrast to the general *attern of su.di4ision of di4ersity across continents :5' -n other s*ecies, co+*rehensi4e studies of geogra*hical *atterns of genetic di4ersity ha4e either yet to .e *u.lished or the results see+ to .e 4ery different' -n horses, for e!a+*le, there is so+e association .et=een +itochondrial lineages and geogra*hy' "or e!a+*le, northern 0uro*ean *onies share a distinct +itochondrial lineage, as do -.erian and north=est 1frican .reeds 13' >o=e4er, it is hard to discern other o.4ious geogra*hic *atterns in horse genetic di4ersity' 1s =ith goats, this is likely to .e the result of the e!tensi4e +o4e+ent of horses' -n fact, horses ha4e e!tre+ely lo= intercontinental *o*ulation differentiation @as assessed .y 1M P1A co+*ared to other li4estock s*ecies, =hich is consistent =ith their use +ainly for trans*ortation @1' Be?a8Pereira and ,'%', un*u.lished dataA' -n 0uro*ean *ig .reeds, such as the %arge ;hite and %andrace, ha*loty*es of the 1sian =ild .oar are found as a result of recent introgression, * during .reeding *rogra++es 5#' So, in su++ary, the co+.ined effects of *orta.ilityS+o.ility on the one hand @goats and horsesA and introgression on the other @cattle, shee* and *igsA has sha*ed the distri.ution of genetic di4ersity that =e see in li4estock on a scale today' $he 3uestion therefore arises, =hat kind of di4ersity do =e =ish to conser4e in these s*ecies, and =hat de+ogra*hic and genetic *rocesses do =e ho*e to facilitate in the futureO I+"*&!at&o# 'or !o# er)at&o# $he i+*lications of the +any recent +olecular genetic studies for different do+estic s*ecies are clearly different in each case' >o=e4er, the rele4ance of this infor+ation and ho= it +ight .e incor*orated in +anage+ent *lans for endangered li4estock has so+e general i+*lications' "irst, although the =ild *rogenitor s*ecies are e!tinct for so+e s*ecies @such as cattle and horsesA, the identification of ancestral *o*ulations for other li4estock could .e 4ery i+*ortant for t=o reasons' -t is *ro.a.le that so+e are endangered @for e!a+*le, the 4icuKaA and such infor+ation +ight gi4e e!tra i+*etus for their conser4ation' Moreo4er, ancestral *o*ulations @and closely related s*eciesA +ight .e a source of alleles of econo+ic 4alue that ha4e .een lost .y chance during do+estication 59, 59' -n addition, in s*ecies for =hich do+estication has occurred in .oth the 0ast and the ;est @for e!a+*le, cattle and *igsA, ancestor *o*ulations +ight .e genetically highly di4ergent and the use of these resources +ust take this fact into account' Clearly, care +ust .e taken =hen using these *recious .ut i+*erilled *o*ulations to ensure that they are conser4ed' Second, the characteriBation of genetic di4ersity =ithin and .et=een .reeds, and the identification of the geogra*hical co+*onent of this 4ariation, allo=s region8s*ecific conser4ation +easures to .e *ut in *lace' "or so+e do+estic s*ecies in 0urasia, the eastern8+ost .reeds or those nearest the *utati4e centres of do+estication ha4e re*eatedly .een sho=n to contain greater genetic di4ersity than .reeds located further a=ay fro+ these *oints' Manage+ent strategies and *riorities for the +aintenance of genetic di4ersity +ust not ignore these dataE these higher di4ersity .reeds should recei4e a conco+itant higher *riority for conser4ation' -n a *hylogenetic sense, so+e i+*ortant disco4eries ha4e .een +ade that a**arently rule out certain candidate s*ecies as *otential *rogenitors of +odern li4estock' "or e!a+*le, neither the =ild urial or the argali are likely to .e the *rogenitors of shee* :D and the guanaco al+ost certainly did not gi4e rise to the al*aca @although it has +ade so+e genetic contri.utionA 31' Con4ersely, such studies ha4e successfully identified s*ecies that should .e a *riority for conser4ation .ecause they re*resent the +ost likely *rogenitors of li4estock 51' -n this conte!t, the relati4e *aucity of infor+ation on genetic di4ersity in 1sian *o*ulations of li4estock and their *utati4e ancestors needs to .e addressed, gi4en the general *attern of 0astH;est di4ergence in se4eral s*ecies' -n other s*ecies, for =hich the =ild *rogenitors ha4e still to .e identified or are already e!tinct, the 4alue of *hylogenetics in their conser4ation is less clear' "urther+ore, o=ing to the e!tensi4e effects of introgression in +odern li4estock and the lack of concordance .et=een different genetic +arkers in +any studies, so+e of the =idely used *hylogenetic units of conser4ation that ha4e .een de4elo*ed for =ild s*ecies, such as the 0P %&$- 615-%I S-,6-"-C16$ &6-$ and the M161,0M06$ &6-$D#, see+ ina**lica.le' $he e!tensi4e =ithin8.reed di4ersity and the often contradictory =ay in =hich different +olecular +arkers segregate in do+estic s*ecies *oses s*ecial challenges for 1n,5 conser4ation in li4estock' 5ecently, the a**lication of di4ersity8.ased +ethods for *rioritiBing li4estock .reeds for conser4ation has centred on the use of the /;eitB+an 1**roach/ D1' ;eitB+an/s conce*t in4ol4es a /di4ersity function/, =hich is the di4ersity enco+*assed .y a set of .reeds under econo+ic consideration for conser4ation' $o .eco+e a *riority for conser4ation any ne= .reed that is to .e added to the list +ust add ne= di4ersity ele+ents' $his e!tra di4ersity +ight .e su++ariBed .y *air=ise genetic distances =ith the e!isting .reeds in the set and .e re*resented in a cluster analysis or as *art of a dendrogra+' Breeds that add the highest o4erall genetic distance to the re+ainder of the set @and =hich should .e located at the ti*s of the +ost distinct and longest .ranches of the dendrogra+A =ould .e gi4en the highest *riority for conser4ation' >o=e4er, .y su++ariBing .reed di4ersity to a single genetic distance +easure this a**roach fails to account ade3uately for the di4ersity and geogra*hical structure that can .e found =ithin so+e .reeds' -t also fails to take into account the fact that genetic distance esti+ates =ill 4ary greatly according to the +arker used and the recent de+ogra*hic history of the .reed @for e!a+*le, =hether it has *assed through a *o*ulation .ottleneckA' "or e!a+*le, a se4erely .ottlenecked .reed =ill ha4e a large genetic distance o=ing to genetic drift, .ut often =ill contain little genetic di4ersity relati4e to other .reeds' Future $&re!t&o# 1 great challenge a=aits li4estock conser4ationists =ho =ish to use +olecular data in the future' $he co+*le!ity of accounting for the *hylogenetic co+*onent of di4ersity in +odern .reeds and the need to +aintain desired le4els of 4ariation =ithin those .reeds could *roduce conflicting +anage+ent strategies' $herefore, the integration of these ai+s into a general +anage+ent a**roach to conser4e 1n,5 +ight not .e *ossi.le or e4en desira.le' >o=e4er, to effecti4ely docu+ent and conser4e di4ersity =ithin and .et=een .reeds, it see+s i+*erati4e that different +arker ty*es are used to assay 4ariation' $he utility of +t)61 and +icrosatellites has .een discussed in this re4ie=, .ut gi4en the huge influence that +ale8+ediated gene flo= can ha4e on di4ersity at often 4ery large s*atial scales (D, I8chro+oso+e +arkers =ill .e highly influential in genetic +anage+ent studies of the futureD(' 1t *resent, ho=e4er, the +olecular +arkers used to characteriBe di4ersity in li4estock ha4e little to do =ith the genes under selection for econo+ically i+*ortant traits' $he identification of causati4e +utations for *henoty*ic 4ariation =ill add a ne= di+ension to the characteriBation of ani+al do+estication, as it =ill allo= researchers to trace selection and the s*read of econo+ically i+*ortant alleles' Such

analysis is *otentially 4ery *o=erful, es*ecially =hen co+.ined =ith single nucleotide *oly+or*his+ @S6PA screening +ethods, and indicates that there are e!citing ne= a4enues of research in this areaD3' ;ith the *u.lication of geno+e se3uences for key do+estic s*ecies due in the near future and the increasing a4aila.ility of e!*ressed se3uence tag @0S$A data.ases, the *ros*ects look good for an e!*onential increase in the a4aila.ility of *oly+or*hic +arkers of .oth neutral and selected 4arieties' -t is e!citing that in the future =e should .e a.le to si+ultaneously detect +ale and fe+ale de+ogra*hic history and the signatures of selection, *ast and *resent, =ithin the geno+es of our do+estic li4estock' 1d4ances in ancient8)61 a**roaches and colla.orations .et=een geneticists and archaeologists =ill ad4ance li4estock do+estication studies and enhance our a.ility to infer their e4olutionary and de+ogra*hic history:(, :3' 1ncient )61 =ill hel* us to *in*oint the geogra*hic locations of origin for the different li4estock lineages, and to deter+ine the ti+ing and routes of their s*read across the ld ;orld' "inally, the use of +olecular +arkers, in co+.ination =ith a di4ersity a**roach that is .ased on ;eitB+an/s +odelD1, *ro+ises to offer a rational =ay ahead and to re4eal in +ore detail the genetic di4ersity in li4estock *o*ulations that are in increasing need of genetic +anage+ent'


Bo! 1 J Mitochondrial )61 in li4estock studies

Mitochondrial @+tA )61 is routinely used to *roduce *hylogenetic trees at se4eral ta!ono+ic le4els, fro+ =ithin s*ecies to a+ong orders of +a++als' -n li4estock it has .een used to descri.e 4ariation in *utati4e =ild ancestor *o*ulations and +odern do+estic *o*ulations'

Both the cytochro+e b gene and the control region C a highly 4aria.le section of +t)61 C are used .ecause these fast e4ol4ing loci are .est suited to e!a+ining 4ariation at the s*ecies le4el or .elo=' C-to!hro+e b $his gene has *ro4en to .e es*ecially i+*ortant in li4estock studies (:, 31 .ecause its te+*o and +ode of e4olution is =ell understood and is thought to .e relati4ely constant and si+ilar a+ong large8.odied terrestrial +a++als D:' "or e!a+*le, in shee* @Ovis ariesA and goats @Capra hircusA, cytochro+e b e4ol4es at a rate .et=een 3'9 and 5':Q *er +illion years, de*ending on the inter*retation of the fossil record (:' Conse3uently, cytochro+e b, rather than the control region, is often used in con?unction =ith the fossil record to /cali.rate/ a M %0C&%15 C% CK a+ong +itochondrial )61 lineages in li4estock' Co#tro* re(&o# $he control region sho=s e!traordinary le4els of 4ariation =ithin s*ecies, =hich +eans that it can .e used to track geogra*hic *atterns of di4ersity and e4olution @/*hylogeogra*hy/ D5A, dis*ersal, gene flo=, de+ogra*hic e!*ansion, genetic drift and hy.ridiBation' $he use of standard *hylogenetic trees to descri.e the +ost likely e4olutionary relationshi* a+ong ha*loty*es has dra=.acks =ithin s*ecies and es*ecially in li4estock H *ri+arily o=ing to *arallel +utations and reticulation @lineage e!change .et=een di4ergent *o*ulationsA' So, *hylogenetic trees ha4e .een aug+ented .y /net=orks/' -n a net=ork, the ha*loty*e se3uence is re*resented as a node and the genetic distance a+ong nearest8 neigh.our ha*loty*es scales the length of the .ranch connecting the+ DD, DF' ne ad4antage of this a**roach is the a.ility to gra*hically illustrate alternati4e, e3ually *ro.a.le connections a+ong ha*loty*es on the sa+e net=ork @for e!a+*le, see "ig' (.A' Most i+*ortantly it is the high rate of e4olutionary change and the a.ility to detect differentiation .et=een do+estic lineages that +akes the control region the +ethod of choice for li4estock studies' $he recent use of /+is+atch distri.utions/ can test different +odels of de+ogra*hic e!*ansion that are e!*ected to acco+*any do+estication .y +an' $his is done .y e!a+ining the distri.ution of *air=ise differences .et=een ha*loty*es =ithin a *o*ulationD9' 1 recent analysis of +is+atch distri.utions in do+estic goats *ro4ides a good e!a+*le @see figureA' $he *attern .est fitting a recent +arked de+ogra*hic e!*ansion is the one seen in the figure, in =hich +ost ha*loty*es are se*arated .y only a fe= su.stitutions .ecause there has not .een enough e4olutionary ti+e for a large to accu+ulate co+*ared =ith the rate of *o*ulation increase' -n addition, a te+*oral ele+ent can .e added to the analysis and C hircus ha*logrou* 1 is *redicted to ha4e started e!*anding first @it has the +ost *air=ise +is+atchesA, follo=ed .y ha*logrou* C and then ha*logrou* B(:' $he figure is re*roduced =ith *er+ission fro+ 5ef' (: M 6ational 1cade+y of Sciences, &S1 @(##1A'

Bo! ( J Microsatellites as nuclear +arkers of do+estic origins

$he fre3uency distri.utions of different siBed alleles for the +icrosatellite locus I;%%:D are sho=n in the t=o *utati4e =ild ancestors of the +odern8day lla+a @ Lama glamaA and al*aca @Vicugna pacosA, the 4icuKa @Vicugna vicugnaA and guanaco @Lama guanicoeA' 1llele siBes do not o4erla* .et=een the t=o =ild s*ecies @see figure, *art aA' >o=e4er, although the allele siBe distri.utions in al*aca +atch closely to that of the 4icuKa and those in the lla+a si+ilarly +atch that of the guanaco, the +ost co++on guanaco allele is found in al*aca and the +ost co++on 4icuKa allele is found in lla+a @see figure, *art bA, =hich indicates that there has .een .idirectional hy.ridiBation'

$hese results are in total contrast to the +itochondrial data, for =hich the +a?ority of .oth lla+a and al*aca ha4e a +itochondrial ha*logrou* that indicates a guanaco ancestry' )eli.erate hy.ridiBation of al*aca +ales =ith lla+a fe+ales to increase .ody siBe and fleece =eight, follo=ed .y su.se3uent .ackcrossing =ith al*aca +ales to *roduce a finer is one *ossi.le e!*lanation for this *attern' $his figure is re*roduced =ith *er+ission fro+ 5ef' 31 M $he 5oyal Society @(##1A'

F8RTHER INFORMATION "ood and 1griculture rganiBation of the &nited 6ations J (##( -&C6 5ed %ist of $hreatened S*ecies


1' Sala+ini, "', TBkan, >', Brandolini, 1', SchUfer8Pregl, 5' V Martin, ;' ,enetics and geogra*hy of =ild cereal do+estication in the near east' !ature "ev #enet 3, :(9H::1 @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J (' Mac>ugh, )' 0' V Bradley, )' ,' ,oats .uck the trend' $roc !atl %cad Sci &S% 9:, 539(H539: @(##1A' J 1rticle J Pu.Med J Che+Port J 3' ,oldstein, )' B' V Chikhi, %' >u+an +igrations and *o*ulation structureE =hat =e kno= and =hy it +atters' %nnu "ev #enomics 'um #enet 3, 1(9H15( @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J :' Sa4olainen, P', Ghang, I' P', %u, 7', %unde.erg, 7' V %eitner, $' ,enetic e4idence for an 0ast 1sian origin of do+estic dogs' Science 29:, 1D1#H1D13 @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J 5' 5osen.erg, 6' 1' et al' 0+*irical e4aluation of genetic clustering +ethods using +ultilocus genoty*es fro+ (# chicken .reeds, #enetics 1;9, D99HF13 @(##1A' J Pu.Med J -S- J Che+Port J D' "ood and 1griculture rganiBation of the &nited 6ations' Secondar( #uidelines for the )evelopment of !ational *arm %nimal #enetic "esources +anagement, +anagement of Small $opulations at "isk' @"ood and 1griculture rganiBation, 5o+e, 1999A' F' "roufe, 0', Magyary, -', %ehocBky, -' V ;eiss, S' Mt)61 se3uence data su**orts an 1sian ancestry and single introduction of the co++on car* into the )anu.e .asin' - *ish Biol <1, 3#1H3#: @(##(A' J 1rticle J -S- J Che+Port J 9' Blu+ler, M' 1' -nde*endent in4entionis+ and recent genetic e4idence on *lant do+estication' Econ Bot =<, 99H111 @199(A' J -S- J 9' Sherratt, 1' Cli+atic cycles and .eha4ioural re4olutionsE the e+ergence of +odern hu+ans and the .eginning of far+ing' %ntiquit( >1, (F1H (9F @199FA' J -S- J 1#' Kealhofer, %' Changing *erce*tions of riskE the de4elo*+ent of agro8ecosyste+s in Southeast 1sia' %m %nthropol 1?=, 1F9H19: @(##(A' J -S- J 11' )ia+ond, 7' 04olution, conse3uences and future of *lant and ani+al do+estication' !ature =1:, F##HF#F @(##(A' Th& re)&e/ u++ar&@e a#$ -#the &@e the $&''ere#t a#$ !o+"*e+e#tar- ,&#$ o' $ata A(e#et&!4 *a#(u& t&!4 ar!haeo@oo*o(&!a* a#$ o o#B that are be&#( u e$ to &#'er the or&(&# a#$ "rea$ o' $o+e t&! a(r&!u*tura* "*a#t a#$ a#&+a* 1 J 1rticle J Pu.Med J -S- J Che+Port J 1(' 5icherson, P' 7', Boyd, 5' V Bettinger, 5' %' ;as agriculture i+*ossi.le during the Pleistocene .ut +andatory during the >oloceneO 1 cli+ate change hy*othesis' %m %ntiq <<, 39FH:11 @(##1A' J -S- J 13' 7ansen, $' et al' Mitochondrial )61 and the origins of the do+estic horse' $roc !atl %cad Sci &S% 99, 1#9#5H1#91# @(##(A' J 1rticle J Pu.Med J Che+Port J 1:' Pila, C' et al' ;ides*read origins of do+estic horse lineages' Science 291, :F:H:FF @(##1A' J 1rticle J Pu.Med J -S- J Che+Port J

15' Balasse, M', Bocherens, >', $resset, 1', Mariotti, 1' V Pigne, 7' )' 0+ergence of dairy *roduction in the 6eolithicO Contri.ution of isoto*ic analysis of cattle archaeological .ones' Comptes "endus %cad Sci Ser .. 32;, 1##5H1#1# @199FA' J 1rticle J -S- J 1D' 1l4ard, M' S' V KuBnar, %' )eferred har4estsE the transition fro+ hunting to ani+al hus.andry' %m %nthropol 1?3, (95H311 @(##1A' J -S- J

1F' Geder, M' 1' V >esse, B' $he initial do+estication of goats @Capra hircusA in the Gagros +ountains 1#,### years ago' Science 2:>, ((5:H ((5F @(###A' Th& "a"er u e #u+erou "re!& e !arbo# $ate a#$ a h&'t &# $e+o(ra"h&! "ro'&*e Aa(e a#$ e. o' har)e te$ +a*e B 'ro+ (oat 'o &* +ater&a* to "ro)&$e o+e o' the o*$e t a#$ be t e)&$e#!e 'or (oat $o+e t&!at&o# a*o#( the bor$er o' Ira3 a#$ Ira#1 J 1rticle J Pu.Med J -S- J Che+Port J 19' Mannion, 1' M' )o+estication and the origins of agricultureE an a**raisal' $h(s #eog 23, 3FH5D @1999A' J 1rticle J

19' Kar*, 1' et al' Molecular technologies for .iodi4ersity e4aluationE o**ortunities and challenges' !ature Biotech 1;, D(5HD(9 @199FA' J Pu.Med J -S- J Che+Port J (#' Sunnucks, P' 0fficient genetic +arkers for *o*ulation .iology /rends Ecol Evol 1;, 199H(#3 @(###A' J 1rticle J Pu.Med J -S- J

(1' %oftus, 5' $', Mac>ugh, )' 0', Bradley, )' ,', Shar*, P' M' V Cunningha+, P' 04idence for t=o inde*endent do+estications of cattle' $roc !atl %cad Sci &S% 91, (F5FH(FD1 @199:A' Th& "a"er /a the '&r t &# a er&e o' &#)e t&(at&o# o' $o+e t&! a#&+a* that "o&#te$ to/ar$ #u+erou (eo(ra"h&!a**e"arate$ $o+e t&!at&o# 1 J Pu.Med J Che+Port J ((' Mac>ugh, )' 0', %oftus, 5' $', Bradley, )' ,', Shar*, P' M' V Cunningha+, P' Microsatellite )61 4ariation =ithin and a+ong 0uro*ean cattle .reeds' $roc " Soc Lond B 2;<, (5H31 @199:A' J Pu.Med J -S- J Che+Port J (3' >andt, ', Meyer, S' V 4on >aeseler, 1' Co+*ilation of hu+an +t)61 control region se3uences' !ucleic %cids "es 2<, 1(DH1(9 @1999A' J 1rticle J Pu.Med J -S- J Che+Port J (:' %uikart, ,' et al' Multi*le +aternal origins and =eak *hylogeogra*hic structure in do+estic goats' $roc !atl %cad Sci &S% 9:, 59(FH593( @(##1A' Th& tu$- $ete!te$ e.tre+e*- h&(h +tDNA $&)er &t- a#$ ur"r& &#(*- *&tt*e &#ter!o#t&#e#ta* $&''ere#t&at&o# &# (oat a !o+"are$ to !att*e a#$ hee"1 It &$e#t&'&e$ three "ote#t&a* or&(&# Athat & 4 three $&)er(e#t +tDNA *&#ea(e B4 &#!*u$&#( o#e 'ro+ outh or ea t A &a4 a#$ u((e te$ a# e+er(&#( "atter# o' Ea tC0e t $ua* $o+e t&!at&o# &# 'ar+ a#&+a* 1 J 1rticle J Pu.Med J Che+Port J (5' 14ise, 7' C' +olecular +arkers0 !atural 'istor( and Evolution @Klu=er 1cade+ic, Boston, M1, 1993A'

(D' Mac>ugh, )' 0', Shri4er, M' )', %oftus, 5' $', Cunningha+, P' V Bradley, )' ,' Microsatellite )61 4ariation and the e4olution, do+estication and *hylogeogra*hy of taurine and Be.u cattle @Bos taurus and Bos indicus A' #enetics 1=<, 1#F1H1#9D @199FA' The #o)e*t- o' th& /or, /a the u#!ou"*&#( o' "ater#a* a#$ +ater#a* *&#ea(e &# $o+e t&! "o"u*at&o# (e#et&! h& tor-1 A'r&!a# !att*e "o"u*at&o# ho/ ub ta#t&a* Bos indicus a#!e tr- &# the&r Y !hro+o o+e a#$ auto o+e 4 but *a!, a#- +tDNA )ar&a#t 'ro+ that ta.o#1 J Pu.Med J -S- J Che+Port J (F' Bunt?er, 7' B', tsen, M', 6i?+an, -' 7', Kui*er, M' $' 5' V %enstra, 7' 1' Phylogeny of .o4ine s*ecies .ased on 1"%P finger*rinting' 'eredit( ::, :DH51 @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J (9' 1?+one Marsan, P' et al' ,enetic distances =ithin and across cattle .reeds as indicated .y .iallelic 1"%P +arkers' %nim #enet 33, (9#H(9D @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J (9' Bruford, M' ;' V ;ayne, 5' K' Microsatellites and their a**lication to *o*ulation genetics' Curr Opin #enet )ev 3, 939H9:3 @1993A' J Pu.Med J Che+Port J 3#' )ieB8$ascWn, C', %ittle?ohn, 5' P', 1l+eida, P' 1' 5' V Cra=ford, 1' M' ,enetic 4ariation =ithin the Merino shee* .reedE analysis of closely related *o*ulations using +icrosatellites' %nim #enet 31, (:3H(51 @(###A' J 1rticle J Pu.Med J -S- J 31' Kad=ell, M' et al' ,enetic analysis re4eals the =ild ancestors of the lla+a and al*aca' $roc " Soc Lond B 2<:, (5F5H(59: @(##1A' Th& tu$- &#te(rate$ +tDNA a#$ +&!ro ate**&te a#a*- e to e*u!&$ate the or&(&# o' South A+er&!a# *&)e to!, $e "&te the&r re!urre#t h-br&$&@at&o#1 J 1rticle J Pu.Med J -S- J Che+Port J 3(' Matsuoka, I' et al' 1 single do+estication for +aiBe sho=n .y +ultilocus +icrosatellite genoty*ing' $roc !atl %cad Sci &S% 99, D#9#HD#9: @(##(A' J 1rticle J Pu.Med J Che+Port J 33' Cornuet, 7' M', Piry, S', %uikart, ,', 0stou*, 1' V Solignac, M' 6e= +ethods e+*loying +ultilocus genoty*es to select or e!clude *o*ulations as origins of indi4iduals' #enetics 1;3, 1999H(### @1999A' J Pu.Med J -S- J Che+Port J 3:' Maudet, C', %uikart, ,' V $a.erlet, P' ,enetic di4ersity and assign+ent tests a+ong se4en "rench cattle .reeds .ased on +icrosatellite )61 analysis' - %nim Sci :?, 9:(H95# @(##(A' J Pu.Med J -S- J Che+Port J

35' %uikart, ,' V Cornuet, 7' 8M' 0+*irical e4aluation of a test for detecting recent historical *o*ulation .ottlenecks' Conserv Biol 12, ((9H(3F @1999A' J 1rticle J -S- J 3D' Stanley, >' "', Kad=ell, M' V ;heeler, 7' C' Molecular e4olution of the fa+ily Ca+elidaeE a +itochondrial study' $roc " Soc Lond B 2;<, 1H D @199:A' J Pu.Med J -S- J Che+Port J 3F' ;heeler, 7' C' 04olution and *resent situation of the South 1+erican Ca+elidae' Biol - Linn Soc ;=, (F1H(95 @1995A' J -S- J

39' Bradley, )' ,', Mac>ugh, )' 0', Cunningha+, P' V %oftus, 5' $' Mitochondrial di4ersity and the origins of 1frican and 0uro*ean cattle' $roc !atl %cad Sci &S% 93, 5131H5135 @199DA' J 1rticle J Pu.Med J Che+Port J 39' %oftus, 5' $' et al' Mitochondrial genetic 4ariation in 0uro*ean, 1frican and -ndian cattle *o*ulations' %nim #enet 2;, (D5H(F1 @199:A' J Pu.Med J -S- J Che+Port J :#' Perkins, )', 7r' "auna of Xatal >YyYkE e4idence for early cattle do+estication in 1natolia' Science 1<=, 1FFH1F9 @19D9A' J Pu.Med J -S- J

:1' Pernesi, C' et al' ,enetic characteriBation of the .ody attri.uted to the e4angelist %uke' $roc !atl %cad Sci &S% 9:, 13:D#H13:D3 @(##1A' J 1rticle J Pu.Med J Che+Port J :(' $roy, C' S' et al' ,enetic e4idence for 6ear80astern origins of 0uro*ean cattle' !ature =1?, 1#99H1#91 @(##1A' A#!&e#t a#$ +o$er# +tDNA "h-*o(eo(ra"h- &# Euro"ea# !att*e &#$&!ate a $er&)e$ or&(&# 'ro+ the Near Ea t a#$ u""ort a $&''ere#t h& tor- 'or A'r&!a# !att*e1 J 1rticle J Pu.Med J -S- J Che+Port J :3' %eonard, 7' 1' et al' 1ncient )61 e4idence for @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J ld ;orld origin of 6e= ;orld dogs' Science 29:, 1D13H1D1D

::' %ister, 1' M' et al' 1ncient and +odern )61 fro+ a 4ariety of sources in a study of horse do+estication' %nc Biomol 2, (DFH(9# @1999A' J Che+Port J :5' >iendleder, S', MainB, K', Plante, I' V %e=alski, >' 1nalysis of +itochondrial )61 indicates that do+estic shee* are deri4ed fro+ t=o ancestral +aternal sourcesE no e4idence for contri.utions fro+ urial and argali shee*' - 'ered :9, 113H1(# @1999A' J 1rticle J Pu.Med J -S- J Che+Port J :D' >iendleder, S', Kau*e, B', ;ass+uth, 5' V 7anke, 1' Molecular analysis of =ild and do+estic shee* 3uestions current no+enclature and *ro4ides e4idence for do+estication fro+ t=o different su.s*ecies' $roc " Soc Lond B 2<9, 993H9#: @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J :F' %au, C' >' et al' ,enetic di4ersity of 1sian =ater .uffalo @Bubalus bubalisAE +itochondrial )8loo* and cytochro+e b se3uence 4ariation' %nim #enet 29, (53H(D: @1999A' J 1rticle J Pu.Med J -S- J Che+Port J :9' $anaka, K' et al' Phylogenetic relationshi* a+ong all li4ing s*ecies of the genus Bubalus .ased on )61 se3uences of the cytochro+e b gene' Biochem #enet 3=, ::3H:5( @199DA' J Pu.Med J -S- J Che+Port J :9' ,uiffra, 0' et al' $he origin of the do+estic *igE inde*endent do+estication and su.se3uent introgression' #enetics 1;=, 1F95H1F91 @(###A' A !*ear &**u trat&o# o' the e"arat&o# o' the ea ter# a#$ /e ter# !*a$e o' $o+e t&! "&(4 &#!*u$&#( !o+"ar& o# o' both +tDNA a#$ #u!*ear (e#e e3ue#!e 1 J Pu.Med J Che+Port J 5#' Ki?as, 7' M' >' V 1ndersson, %' 1 *hylogenetic study of the origin of the do+estic *ig esti+ated fro+ the near8co+*lete +t)61 geno+e' +ol Evol ;2, 3#(H3#9 @(##1A' J Pu.Med J -S- J Che+Port J 51' ;atano.e, $' et al' Prehistoric introduction of do+estic *igs onto the (((H(31 @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J kina=a islandsE ancient +itochondrial )61 e4idence' - +ol Evol ;;,

5(' $o=nsend, S' 7' #enetic diversit( and domestication in sheep 1Ovis2' $hesis, &ni4' 0ast 1nglia @(###A'

53' Ki+, K' -', %ee, 7' >', %ee, S' S' V Iang, I' >' Phylogenetic relationshi*s of northeast 1sian cattle to other cattle *o*ulations deter+ined using +itochondrial )61 )8loo* se3uence *oly+or*his+' Biochem #enet =1, 91H99 @(##3A' J 1rticle J Pu.Med J -S- J Che+Port J 5:' Kikka=a, I' et al' Phylogenies using +t)61 and S5I *ro4ide e4idence for +ale8+ediated introgression in 1sian do+estic cattle' %nim #enet 3=, 9DH1#1 @(##3A' J Pu.Med J -S- J Che+Port J 55' Miretti, M' M', Pereira, >' 1', Poli, M' 1', Contel, 0' P' B' V "erro, 7' 1' 1frican8deri4ed +itochondria in South 1+erican nati4e cattle .reeds @Bos taurusAE e4idence of a ne= taurine +itochondrial lineage' - 'ered 93, 3(3H33# @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J 5D' >anotte, ' et al' 1frican *astoralis+E genetic i+*rints of origins and +igrations' Science 29<, 33DH339 @(##(A' Th& a""*&e$ the -#thet&! +a" a""roa!h o' Ca)a**&7S'or@a a#$ !o**ea(ue to !att*e $&)er &t- o# a /e**7 a+"*e$ !o#t&#e#t a#$ u#!o)ere$ e"arate a#$ &#ter"retab*e *e)e* o' (e#et&! )ar&at&o#1 J 1rticle J Pu.Med J -S- J Che+Port J

5F' ;ood, 6' 7' V Phua, S' >' Pariation in the control region se3uence of the shee* +itochondrial geno+e' %nim #enet 2>, (5H33 @199DA' J Pu.Med J -S- J Che+Port J 59' Porter, P' #oats of the 3orld @"ar+ing Press, -*s=ich, &K, 199DA'

59' Ier!at, M' I' 1**lication of =ild goats in cash+ere .reeding' Small "uminant "es 1;, (9FH(91 @1995A' J 1rticle J -S- J

D#' MoritB, C' 1**lications of +itochondrial )61 analysis in conser4ation C a critical re4ie=' +ol Ecol 3, :#1H:11 @199:A' J -S- J Che+Port J

D1' ;eitB+an, S' / n di4ersity/' 4uart - Econ 1?>, 3D3H:#5 @199(A' J -S- J

D(' >anotte, ' et al' ,eogra*hic distri.ution and fre3uency of a taurine Bos taurus and an indicine Bos indicus I s*ecific allele a+ongst su.8 Saharan 1frican cattle .reeds' +ol Ecol 9, 39FH39D @(###A' J 1rticle J Pu.Med J -S- J Che+Port J D3' >eaton, M' P' et al' Selection and use of S6P +arkers for ani+al identification and *aternity analysis in &S .eef cattle' +amm #enome 13, (F(H(91 @(##(A' J 1rticle J Pu.Med J -S- J Che+Port J D:' -r=in, )' M', Kocher, $' )' V ;ilson, 1' C' 04olution of the cytochro+e8 b gene of +a++als' - +ol Evol 32, 1(9H1:: @1991A' J Pu.Med J -S- J Che+Port J D5' 14ise, 7' C' $h(logeograph(, /he 'istor( and *ormation of Species @>ar4ard &ni4' Press, >ar4ard, (###A'

DD' Bandelt, >' 7', "orster, P', Sykes, B' C' V 5ichards, M' B' Mitochondrial *ortraits of hu+an *o*ulations using +edian net=orks' #enetics 1=1, F:3HF53 @1995A' J Pu.Med J -S- J Che+Port J DF' Bandelt, >' 7', "orster, P' V 5Zhl, 1' Median ?oining net=orks for inferring intras*ecific *hylogenies' +ol Biol Evol 1<, 3FH:9 @1999A' J Pu.Med J -S- J Che+Port J D9' 5ogers, 1' 5' V >ar*ending, >' Po*ulation gro=th +akes =a4es in the distri.ution of *air=ise genetic differences' +ol Biol Evol 9, 55(H5D9 @199(A' J Pu.Med J -S- J Che+Port J D9' %oftus, 5' $' et al' 1 +icrosatellite sur4ey of cattle fro+ a centre of originE the 6ear 0ast' +ol Ecol :, (#15H(#(( @1999A' J 1rticle J Pu.Med J -S- J Che+Port J F#' Stein.orn, 5' et al' Coe!istence of Bos taurus and Bos indicus +itochondrial )61s in nuclear transfer8deri4ed so+atic cattle clones' #enetics 1<2, 9(3H9(9 @(##(A' J Pu.Med J -S- J Che+Port J F1' ;atano.e, $' et al' ,enetic relationshi* and distri.ution of the 7a*anese =ild .oar @Sus scrofa leucom(sta5A and 5yukyu =ild .oar @Sus scrofa riukiuanus A analysed .y +itochondrial )61' +ol Ecol :, 15#9H151( @1999A' J 1rticle J Pu.Med J -S- J Che+Port J F(' Bro=n, ;' M', ,eorge, M' and ;ilson, 1' C' 5a*id e4olution of ani+al +itochondrial )61' $roc !atl %cad Sci &S% ><, 19DFH19F1 @19F9A' J Pu.Med J Che+Port J F3' >orai, S', >ayasaka, K', Kondo, 5', $sugane, K' V $akahata, 6' 5ecent 1frican origin of +odern hu+ans re4ealed .y co+*lete se3uences of ho+inid +itochondrial )61s' $roc !atl %cad Sci &S% 92, 53(H53D @1995A' J Pu.Med J Che+Port J F:' -&C6SSSC Ca*rinae S*ecialist ,rou*' 3ild Sheep and #oats and their "elatives @Shackleton, )' M', ed'A @,land, S=itBerland and Ca+.ridge, &K, 199FA'

M';'B' =ould like to ackno=ledge funding fro+ the &K Ministry of 1griculture, "isheries and "ood and the 0uro*ean Co++ission @0C 6 ,060 *ro?ectA' S' $o=nsend, K' Byrne, %' Chikhi, ,'M' >e=itt, %' 1lderson, $he 5are Breeds Sur4i4al $rust, 7' ;heeler, 5, 5osadio, M' Kad=ell and M' "ernandeB ha4e all contri.uted significantly to M';'B'/s li4estock research' ,'%' =as su**orted .y grants fro+ 61$ , the ,er+an "ederal 1gency for 6ature Conser4ation @Scientific 1uthority to C-$0SA, the "rench C65SS-6S05M se3uencing *rogra++e and the 0uro*ean Co++ission @0C 6 ,060 *ro?ectA'