MacHugh & Bradley 2001-Domestikacija Koze

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Commentary

Livestock genetic origins: Goats buck the trendDavid E. MacHugh* and Daniel G. Bradley

*Department of Animal Science and Production and Conway Institute of Biomolecular and Biomedical Research, Faculty of Agriculture, University College,Dublin 4, Ireland; and Department of Genetics, Smurfit Institute, Trinity College, Dublin 2, Ireland

The domestic goat (Capra hircus) oftenis dismissed as the poor mans cowfor its ability to thrive on meager fodderand cope with harsh environments. How-ever, this belies the economic and archae-ological importance of the species. Froman agricultural standpoint, the worlds 700million goats provide reliable access tomeat, milk, skins, and fiber for small farm-ersparticularly in developing countries.In addition, accumulating archaeologicalevidence indicates that goats, in the form

of their wild progenitorthe bezoar (Ca- pra aegagrus), were the first wild herbi-vores to be domesticated (Fig. 1). Theses tudies s ugges t that this happened10,000 years ago at the dawn of theNeolithic in the region known as the Fer-tile Crescent (1, 2). Therefore these sturdyanimals may have been the first walkinglarders and by example, could have trig-gered subsequent domestications of thefull repertoire of Euroasian livestock spe-cies that have provided the bulk of theanimal protein consumed by ever-expand-ing human populations.

In this issue of PNAS, Luikart and

colleagues (3) addC. hircus

to the growinglist of domestic animals that have been widely surveyed for mtDNA sequencevariation (49). In their survey, Luikart etal. (3) demonstrate that the structure anddistribution of mtDNA variation in do-mestic goats are qualitatively differentfrom the patterns observed in other largeEurasian herbivores domesticated forfood, skins and fiber (cattle, buffalo, pigs,and sheep; see Fig. 2).

Diversity, Capture, and Genetic Inertia

There has been a long tradition of interestin animal domestic origins among breed-ers, geneticists, and archaeologists. With

the maturation of molecular populationgenetics during the last decade, the toolsare now available to systematically inves-tigate the problem at the phylogeographiclevel. In this regard, mtDNA has repre-sented the most informative genomic el-ement for teasing out the what, where and(admittedly with less confidence), the

when of livestock domestication. Mamma-lian mitochondrial chromosomes display amaternal mode of genetic transmissionand an absence of recombination (10) and

are subject to a relatively rapid mutationrate (particularly in control region se-quences). Because of these genetic fea-tures, mtDNA studies of livestock provide

valuable information about the domesti-cation process.

First, clonal transmission of intactmtDNA haplotypes sans recombinationalnoise means that it is possible to discerndiscrete maternal lineages within domesticpopulations that may have complex ge-netic histories. Consequently, sequencesthat descend from different captures froma diverse wild species maintain a phylo-genetic distinction even after millennia ofdomestic interbreeding. Second, the ratesof substitution accumulation within se-quences of moderate length are of a sim-ilar order to the time depth of domestica-tion. This all ows the res olution of predomestic and postdomestic patterns ofsequence diversityeven allowing for thecalibration difficulties that are inherent incontrol region variation. Third, there

seems to be significant temporal inertia inthe geography of domestic mtDNA. Thehigh disparity between male and femalereproductive variance under managedbreeding implies that maternal lineagesare likely to show some geographical in-ertia, especially with respect to secondaryintrogression. This would suggest that ge-netic change has been predominantlymale-mediated. For example, all Africancattle sampled to date display uniformly Bos taurus mtDNA sequences despite a

widespread and substantial Bos indicusintrogression from the East over severalmillennia (11).

Finally, a widely perceived weakness ofmtDNA phylogeography is that it deals

with only a single segregating locus andone not always representative of the an-cestry of a whole genome. However, in thecontext of animal domestication this mayactually be an advantage. Unlike othergenomic components, a domestic mtDNAlineage must at some point in its historyhave entered the domestic pool throughthe physical capture of a wild female an-imal. Nuclear gene histories may have

been complicated through more ephem-eral encounters between wild males andtame females (as still observed in speciessuch as Asian mithan where the progeni-tor remains accessible).

An East-West Duality in AnimalDomestication?

Fig. 2 shows neighbor-joining trees thatsummarize mtDNA sequence diversity infive domestic ungulate data collections.The most striking feature (with the excep-tion of the horse) is that sequences invari-ably cluster into one of two groups. Thesedistinct clades are separated by a domi-nant internal brancha topology akin to

a double-headed broomstick. A secondimportant feature of the diversity is that,in each case, the two clades have a ten-dency to be geographically distributedprimarily along an East-West division.The phylogenetic divisions within cattleand water buffalo follow (with some qual-

See companion article on page 5927.

To whom reprint requests should be addressed. E-mail:

[email protected].

Fig. 1. A third or fourth century BC Mesopota-

mian stone carving of a man carrying either a do-

mestic or a wild goat. This piece is displayed in the

Louvre Museum in Paris. (Figure courtesy of Mike

Schwartz.)

53825384 PNAS May 8, 2001 vol. 98 no. 10 www.pnas.orgcgidoi10.1073pnas.111163198


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ification) established taxonomic categori-zations based on morphology, i.e., thatbetween humped and humpless cattle andthat between river and swamp buffalo (4,1214). The division in pigs is also be-tween European samples and those from

Asia (8, 15). The pattern in sheep is lessclear, and the sequences used here weresampled from New Zealand herds of nec-essarily exotic origin (16). However withthe corresponding restriction fragmentlength polymorphism haplotypes, one wasfound in a European sheep sample onlyand the second was detected in animals ofboth European and C entral As ian

provenance (7).A third piece of information inherent inthese phylogenies is the quantitative di-

vergence between the dual clades. Underthe assumption of a molecular clock, it ispossible to estimate the coalescence timebetween the two clusters in each species.In each case, the time to the most recentcommon ancestor is estimated in hun-dreds of thousands of years (4, 79, 12, 13,15). Notwithstanding the difficulties incalibrating mtDNA sequence divergence,

particularly within the control region,these estimates comfortably predate thetime depth of domestic history, whichstretches to only ca. 10,000 years ago (17).Finally, in the first four species, the diver-sity within each sister clade is of similarmagnitude, although the numbers sam-pled in each sometimes differ. Thereforetaking these factors into account, the di-

versity within each of the broom-headclusters probably is derived from the at-tenuated sampling of a subset of wild

variation that a domestication event (orseries of localized events) would entail.The extant sequence diversity also would

comprise the limited variation that hasaccrued through mutation within domes-tic history. The quantitative divergencebetween each pair of clusters combined

with their East-West geographical separa-tion provides strong support for at leasttwo domestication centers for cattle,sheep, pig, and water buffalo. The lastspecies, horse, yields a more complex pat-tern that suggests a domestication processon the Eurasian steppes that was not soconstrained within time and space (9).

Domestic Goat Phylogeography

The paper in this issue by Luikart et al. (3)describes the first comprehensive descrip-tion of goat mtDNA variation and bringsclosure to the first phase of molecular studyof the origins of the major Eurasian domes-tic animals. It highlights similarities, but alsointeresting differences with the other Fertile

Crescent species. In the initial part of thestudy, Luikart and his colleagues (3) se-quenced the first hypervariable segment ofthe mtDNA control region from 406 goats,broadly sampled across the Old World.They also analyzed the same mtDNA seg-ment from 14 wild Capra species, includingfour wild bezoar (C. aegagrus). When aphylogenetic tree is constructed from thesedata it suggests that goats, unlike cattle,sheep, or pigs (see Fig. 2) seem to havethree, not two, deep matrilineal roots(termed lineages A, B, and C, respectively).Surprisingly, none of the four C. aegagrussequences emerge within any of these threedomestic haplogroups. However, this may

be an artifact of the small bezoar samplebecause a previous, albeit less comprehen-sive study from the same laboratory hasfound C. aegagrus museum samples that docluster within a C. hircus mtDNA haplo-group (18).

To gain a better understanding of therelationships among the domestic goathaplogroups, Luikart et al. (3) then turnedtheir attention to a region of the mtDNAmolecule that evolves less rapidlythecytochrome b gene. They selected six in-dividual goat samples, two from each ofthe three lineages and obtained complete1,140-bp gene sequences. Using publishedsheep cytochrome b sequences and estab-lished dates for the evolutionary split be-tween Capra and Ovis, Luikart et al. (3)estimate a coalescence time for domesticgoat mtDNA of 200280 thousand yearsago. Armed with this information theyinfer that there were at least three geo-graphically and temporally separate cap-tures of founder female bezoar goats dur-ing the formation of early domesticpopulations. As Luikart et al. (3) demon-strate it is unlikely that a single localdomestication could explain the observedpattern, because the number of reproduc-tively active females necessary to maintainthe three ancestral haplotypes in the

source population would have been im-probably large.Mismatch distribution analysis is a use-

ful statistical method to infer the ancientgenetic demography of a population (19).Luikart et al. (3) use this technique toreveal patterns suggestive of populationexpansion in all three domestic goat lin-eages. Assuming that lineage A (the mostdiverse haplogroup) started expanding

with domestication 10,000 years ago, theythen estimate corresponding expansion

Fig. 2. Unrooted neighbor-joining phylogenies constructed by using uncorrected mtDNA sequence

divergences. Thesedata are as follows: 43 complete cattle control region sequencessampled in disparate

locations onthree continents (4,14); 42 completesheepcontrol region sequences froma mixedbreedNew

Zealand sample (16); 11 partial pig control region sequences that include both East Asian and European

varieties (15); 15 cytochrome b sequences from water buffalo (12, 13); and 18 complete horse control

region sequences (25).

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start points for lineages B and C of about2,000 and 6,000 years ago, respectively.This finding suggests to Luikart et al. (3)that the minor haplogroups derive fromsecondary and tertiary expansions thattrail the initial expansion of lineage A.However, it is important to emphasize thatadditional samples may alter this prelim-inary snapshot of goat genetic history. Inaddition, the wild diversity involved in theoriginal captures may have been quitedifferent. Further work on the phylogeog-raphy within the major haplogroupsshould help to clarify these points.

Another intriguing aspect of Luikart etal.s (3) study is the biogeography of thethree domestic goat mtDNA haplogroups.

Again, the pattern is strikingly differentfrom that observed for cattle, sheep, andpigs. Although we need to keep in mindthe inherent and generally unavoidablebias in sampling, it is clear that lineage Apredominates across the globe (90% ofsamples). Lineage B, on the other hand, is

present in about 6% of the animals sam-pled and seems essentially confined tobreeds from southern Asia. This findingleads Luikart et al. (3) to speculate thatthis lineage may derive from a local do-mestication in the region, perhaps withinthe Neolithic culture of Baluchistan in

western Pakistan. Based on the total sam-ple, lineage C is even rarer, confined to asmall number of European breeds and asingle animal from Mongolia. The ab-sence of lineage C from Near Easternpopulations is puzzling. However, furthersampling, particularly in Central Asia mayshed some light on the origins of thishaplogroup. From a wider perspective,

these rare but distinct lineages raise thepossibility that cryptic legacies of addi-tional domestication may persist within

other domestic species that are less com-prehensively sampled. It therefore may betoo early to presume duality as a paradigmof domestication.

The global distribution of goat mtDNAvariation has an additional surprisea re-markably low level of phylogeographicstructure (particularly when compared withdomestic cattle). In other words, geograph-ical location has little relevance to themtDNA type a particular animal possesses.Based on the antiquity of goat domestica-tion and the documented presence of goatsin all corners of the Old World stretchingdeep into prehistory (20), we might expectthat goats should display relatively high lev-els of geographic structuring. It thereforesuggests to Luikart and his colleagues (rea-sonably in our view), that goats have been ahighly mobile species, probably as small andportable units of human trade throughouthistory (3).

Future Prospects: The Y Imperative

Additional sampling, particularly in re-gions likely to harbor the minor haplo-groups will improve our understanding ofthe where of goat origins. Clearly this isalso necessary in the other mammaliandomesticates and it is apparent that thereis a long way to go before we gain adetailed overview of the biological historyof these important species.

Studies of mtDNA variation, althoughhighly informative, are only one part of thepuzzle. The next phase should be to developsuites of information-rich Y chromosomeDNA markers for each species. Surveys of

variation in the nonrecombining portion ofthis chromosome have been immensely

valuable in complementing and adding tothe picture of recent human evolution thatemerged from mtDNA surveys (21). Fortu-

nately in many cases, animal geneticistsshould be able to short-circuit Y chromo-some marker development. Based on com-parisons with autosomal markers, it is clearthat the rapidly evolving microsatellite-typemarkers developed for one artiodactyl spe-cies often will amplify in other taxa (22, 23).

Once an adequate number of Y-specificsingle-nucleotide polymorphisms and mi-

crosatellites become available for eachdomestic species, they should prove in-

valuable for studies of genetic diversity.These tools will be particularly useful forgoats, where males from any number of

wild populations or subspecies could havecontributed genes to domestic herds. If Yhaplotype systems of sufficient resolutioncan be developed they also should be ableto provide detailed information concern-ing recent geographical movements andperhaps display the breed-specific charac-teristics that mtDNA stubbornly refusesto. Obviously, the autosomal genomeshould not be neglected either and asstudies of microsatellites in cattle have

shown, highly polymorphic diploid mark-ers also can shed light on recent popu-lation movements and reveal the finegrain of admixture between divergentpopulations (11, 24).

The phylogeographic surveys requiredto augment our current knowledge of live-stock diversity will be challenging andexpensive because certain key regions alsomay be the most inaccessible and politi-cally unstable. However, we feel the effort

will be worth it; the genetic origins ofdomestic animals, unlike our own species,are genuinely deep-rooted and multifac-eted and there should be plenty moresurprises in store.

We thank all our colleagues for helpful com-ments and insights. This work was supported bythe Wellcome Trust.

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