A Scheu

CS Troy

DG Bradley

F Racimo

J Schibler

JD Vigne

L Orlando

LA Frantz

Ludovic Orlando

M Schubert

Genome Biology

Crossref

Orlando Genome Biology  (2015) 16:225 DOI 10.1186/s13059-015-0793-zRESEARCH HIGHLIGHT Open AccessThe first aurochs genome reveals thebreeding history of British and European cattleLudovic Orlando1,2See related Research article: www.dx.doi.org/10.1186/s13059-015-0790-2AbstractThe first genome sequence of the extinct Europeanwild aurochs reveals the genetic foundation of nativeBritish and Irish landraces of cattle.parisons between living wild and domestic gene pools.The multiple origins of domestic cattleThe agricultural transition that accompanied theNeolithic Revolution represented a turning point in ourevolutionary history. By domesticating plants and animals,humans no longer depended on foraging and hunting fortheir subsistence and could, for the first time, producetheir own resources, sustaining larger sedentary popula-tions, and ultimately civilizations [1].The domestication of cattle from the now-extinct wildaurochs (Bos primigenius) was essential in this process.Cattle livestock provided us with meat, leather, milk andother dairy products, but also enabled the transportationof goods and people in carts, and considerably helpedthe cultivation of soils by pulling ploughs. The firstarchaeological evidence for wild aurochs domesticationappears in the Anatolian Fertile Crescent around10,500 years ago, where cattle breeding developed forthe next two millennia, before reaching Greece andfurther spreading into Europe [2].The domestication of European taurine cattleEurasian aurochs are well-described in the fossil record,but also on cave paintings, engravings and illustrations.They were one of the largest herbivores in Europe, withthe biggest bulls reaching shoulder heights of 160–180centimeters and massive frontal horns of up to 80 centi-meters. Whether early European farmers fully adoptedCorrespondence: lorlando@snm.ku.dk1Centre for GeoGenetics, Natural History Museum of Denmark, University ofCopenhagen, ØsterVoldgade 5-7, 1350K Copenhagen, Denmark2Université de Toulouse, University Paul Sabatier (UPS), Laboratoire AMIS,CNRS UMR 5288, 37 Allées Jules Guesde, 31000 Toulouse, France© 2015 Orlando. Open Access This article is dInternational License (http://creativecommonsreproduction in any medium, provided you gthe Creative Commons license, and indicate if(http://creativecommons.org/publicdomain/zeMiddle Eastern domestic cattle or incorporated localwild aurochs into their livestock remains contentious. Incontrast to dogs, goats, horses, pigs and sheep, for whichwild populations still exist today, the last B. primigeniusspecimen died in Poland in 1627, precluding direct com-Luckily, the survival of DNA molecules in archaeologicalbones and teeth offers direct access to the geneticmakeup of extinct European wild aurochs, and canthereby help track their possible contribution to theEuropean farming economy.The first comprehensive survey of cattle mitochondrialDNA (mtDNA) variation that included aurochs se-quences was carried out in 2001, and as in any ancientDNA study at the time, consisted of only a few hundredsof nucleotides [3]. The four aurochs analyzed, excavatedin Britain, all belonged to a divergent haplogroup, calledP, virtually absent from modern European breeds (theso-called humpless taurine cattle). Further mtDNA ana-lyses of aurochs from mainland Europe, and ancient do-mestic cattle in the Middle East and throughout Europeconfirmed a unique origin of the European domestictaurine mtDNA lineage in the Fertile Crescent, fromwhich the original captive stock, of perhaps not morethan 80 female founders, later expanded through theDanubian and Mediterranean routes [4]. GeneticmtDNA contact between Europe and the Middle Eastwas virtually lost from 7000 years ago [4], and mostEuropean breeds apparently developed in situ with nomitochondrial influence from local aurochs, exceptperhaps in Italy, Poland and Switzerland where B. primi-genius mtDNA variants can be occasionally found inmodern and/or ancient cattle [5].With high-throughput DNA sequencing technologiesand recent methodological developments in ancientDNA research, whole genomes from ancient individualscan now be reconstructed. This has provided a fan-tastic opportunity to advance our understanding ofistributed under the terms of the Creative Commons Attribution 4.0.org/licenses/by/4.0/), which permits unrestricted use, distribution, andive appropriate credit to the original author(s) and the source, provide a link tochanges were made. The Creative Commons Public Domain Dedication waiverro/1.0/) applies to the data made available in this article, unless otherwise stated.Orlando Genome Biology  (2015) 16:225 Page 2 of 3domestication processes by delivering the genome se-quence of wild animals that lived before domestication.This was done for the first time for horses [6], where wildalleles from a now-extinct wild population could betracked within contemporary domestic breeds, thus re-vealing massive restocking from the wild, and highlightingthe genes that were preferentially selected during domesti-cation. A recent publication in Genome Biology appliesthis approach to cattle and reports the first genome se-quence of a 6700-year-old male aurochs, excavated inDerbyshire, England [7].The first aurochs genomeFrom a total of 3.37 billion Illumina sequence reads,Stephen Park and colleagues [7] could identify 417 millionsequences aligning uniquely and with high confidence tothe cattle reference genome [8]. This represents an aver-age 6.23-fold coverage of the genome, covering about89 % of nucleotide positions at least once, and about 2.1million candidate single-nucleotide polymorphism (SNP)and insertion-deletion (indel) variants. The genetic datasetalso enabled the reconstruction of a high-quality mito-chondrial genome sequence, clustering within the typicalP haplogroup, which is absent from modern British cattlebreeds. This is in line with earlier findings, which origin-ally supported the contention that no British aurochs con-tributed to the genetic makeup of modern British cattle.However, the aurochs nuclear genome revealed a substan-tial amount of admixture with the ancestors of Britishbreeds.The support for this admixture is twofold. First,using the same method that unveiled the presence ofNeanderthal ancestry in the genome of non-Africananatomically modern humans, the authors [7] foundan excess of shared derived polymorphisms betweenthe genome of the aurochs and those of British andIrish breeds, in contrast to those of breeds from main-land Europe. Second, ancestry graphs placed the aur-ochs outside the range of modern taurine cattlediversity, but indicated substantial gene flow into Britishand Irish cattle. Clearly, in contrast to the domesticationmodel built on mtDNA, British and Irish herders appearto have successfully incorporated wild aurochs variationinto their livestock.The limited density of the comparative SNP panelused in these analyses (representing about 15,500 high-quality SNPs genome-wide) precluded an identificationof the aurochs genes that survive within present-dayBritish and Irish cattle. One interesting possibility is thatwild restocking helped adapt domestic cattle to Britainand Ireland, favoring the spread of alleles that had beennaturally selected in local aurochs populations. Suchcases of adaptive introgression have now been demon-strated in anatomically modern humans in Europe andTibet, who acquired alleles from archaic hominins thatwere already adapted to their local environments [9].There is no doubt that the newly released aurochs gen-ome and the massive genome initiative of the 1000 bullgenomes project (http://www.1000bullgenomes.com/) willsoon help investigate whether this was also the case fordomestic European taurine cattle.For now, the authors [7] used shallow genome sequen-cing of 81 modern humpless taurine and indicine(humped zebu cattle, independently domesticated in theIndus valley) cattle to scan for molecular signatures ofpositive selection in the genomes of modern Europeanbreeds. One of these scans focused on loci where theaurochs showed the indicine allele and modern Euro-pean taurine cattle an alternative allele at, or close to,fixation. This revealed 263 loci within potentially regula-tory and protein coding regions, including eight non-synonymous mutations. Interestingly, one of these affectedDGAT1, a gene exhibiting a major quantitative traitnucleotide for milk traits, and known to have been inten-sively selected in dairy cattle populations. Functional clus-tering enrichment analyses showed that genes involved inneurobiology, immunity, growth and metabolism wereover-represented in the 263 variant set, indicating thesebiological processes as key targets of aurochs domestica-tion. Immune genes might, for example, have been essen-tial in the arms race against rapidly evolving pathogens,including those of human origin, as close proximitybetween herders and livestock could now facilitatehost-shifts.PerspectivesAs it provides the first aurochs genome, the study fromPark et al. [7] represents a milestone in cattle genomics.However, it reports the genome of a single British animal,which lived about 4000 years after aurochs were first do-mesticated in the Fertile Crescent. Complete genome se-quencing of early Neolithic aurochs from this region willbe crucial for unraveling the genetic foundation of cattledomestication. As DNA decays at faster rates in warm en-vironments, characterizing such genomes might prove ex-tremely difficult. However, we can be confident that evermore sensitive methods that are tailored to the extractionand manipulation of short DNA molecules [8] will contrib-ute to making this a reality; such methods have alreadyhelped characterize whole mitochondrial and nuclear ge-nomes from much older specimens. Surveying the gen-omic diversity of wild aurochs throughout their wholeEuropean range will be equally important, as mtDNAvariation suggests some population differences betweenmainland Italy and the British Isles. Outside Europe, char-acterizing the genomic variation of African and Asian aur-ochs will also be useful for tracking the origins and geneticmakeup of African taurine and Asian indicine cattle.Orlando Genome Biology  (2015) 16:225 Page 3 of 3The data in hand [7] have revealed that British aurochssignificantly contributed to the genetic makeup of modernBritish and Irish cattle. As such, they reveal local restock-ing from the wild as an important component of cattledomestication, and reject simplistic scenarios where do-mestic livestock were first created in unique domesticationcenters, then expanded, ultimately sweeping away localwild populations. This result is in line with recent findingsin other domestic animals, such as horses, dogs and pigs.It opens intriguing questions about the genetic mecha-nisms enabling maintenance of domestic phenotypes inthe presence of homogenizing gene flow from the wild. Ithas been recently proposed that recurrent selection bybreeders at particular loci underlying domestic traits couldcreate domestication genomic islands maintaining popula-tion differentiation [10]. Future work scanning whole gen-ome panels of wild and domestic ancestors of cattle, dogs,horses and pigs will help identify such regions and, if any,their common features, thereby illuminating the corefeatures of the genetic mechanisms underlying animaldomestication.There is little doubt that ancient genomes willhave an important role in such analyses, as the genepool of domestic animals has been significantlyreshaped within the past 200 years because of in-tense selective breeding and/or cross-breeding ad-mixture, which partly erased genomic signatures ofearlier domestication. Ancient DNA methods providea unique opportunity to bypass such limitations andto chart through space and time the whole history ofgenomic changes accompanying animal domestica-tion. The comparison of selection signatures will alsoreveal which animal traits were preferentially targeted inpast societies.Animal domestication is, however, likely to not justhave remodeled the sequence of the genome. Micro-biomes, for example, might also have changed in relationwith dietary shifts, which possibly affected importantphenotypic traits, ranging from the physiological to thebehavioral. As wild and domestic animals show subtlechanges in brain gene expression networks, transcrip-tional changes are also likely to have been an earlycomponent of domestication. A full comprehension ofanimal domestication will, thus, require extensive meta-genomic, transcriptomic and epigenomic analyses of do-mestic and wild animals, including across developmentalstages and tissues. This will be facilitated by the identifica-tion of functional elements in the genomes of domesticatedanimals being undertaken by the FAANG consortium.Interestingly, ancient DNA will also contribute to such ana-lyses, because new approaches can reveal genome-widemethylation and nucleosome maps [9], thereby providingimportant insights on ancient gene expression levels.It will also be useful because ancient microbiomescan be reconstructed from deep-sequencing data ofcoprolites and dental plaques.Finally, it is important to note that Park and colleagues[7] identified living breeds maximizing local wild ances-try, some of which, such as the Kerry cattle, are pres-ently endangered. Developing conservation plans aimingat preserving such cryptic genetic variation in the Britishand Irish traditional landraces, and designing breedingprograms targeting genomic ancestry blocks of aurochsorigins, might eventually provide an opportunity toreverse-engineer aurochs-like animals, even in the absenceof a proper de-extinction technology.AbbreviationsSNP: Single-nucleotide polymorphism; mtDNA: Mitochondrial DNA.Competing interestsThe author declares that he has no competing interests.References1. Vigne JD. Zooarchaeological aspects of the Neolithic diet transition in theNear East and Europe, and their putative relationships with the NeolithicDemographic Transition. In: BocquetAppel J-P, Bar-Yosef O, editors. TheNeolithic Demographic Transition and its Consequences. New York:Springer Verlag; 2008. p. 179–205.2. Bradley DG, Magee DA. Genetics and the origins of domestic cattle. In:Zeder MA, Bradley DG, Emshwiller E, Smith DB, editors. Documentingdomestication: new genetic and archaeological paradigms. Berkeley:University of California Press; 2006. p. 317–18.3. Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, Cunningham P, et al.Genetic evidence for Near-Eastern origins of European cattle. Nature.2001;410:1088–91.4. Scheu A, Powell A, Bollongino R, Vigne JD, Tresset A, Cakirlar C, et al. Thegenetic prehistory of domesticated cattle from their origin to the spreadacross Europe. BMC Genet. 2015;16:54.5. Schibler J, Elsner J, Schlumbaum A. Incorporation of aurochs into a cattleherd in Neolithic Europe: single event or breeding? Sci Rep. 2014;4:5798.6. Schubert M, Jonsson H, Chang D, Der Sarkissian C, Ermini L, Ginolhac A,et al. Prehistoric genomes reveal the genetic foundation and cost of horsedomestication. Proc Natl Acad Sci U S A. 2014;111:E5661–9.7. Park S, Magee D, McGettigan P, Teasdale M, Edwards C, Lohan AJ, et al.Genome sequencing of the extinct Eurasian wild aurochs, Bos primigenius,illuminates the phylogeography and evolution of cattle. Genome Biol. 2015;In press.8. Orlando L, Gilbert MTP, Willerslev E. Reconstructing ancient genomes andepigenomes. Nat Rev Genet. 2015;16:395–408.9. Racimo F, Sankararaman S, Nielsen R, Huerta-Sanchez E. Evidence for archaicadaptive introgression in humans. Nat Rev Genet. 2015;16:359–71.10. Frantz LA, Schraiber JG, Madsen O, Megens HJ, Cagan A, Bosse M, et al.Evidence of long-term gene flow and selection during domestication fromanalyses of Eurasian wild and domestic pig genomes. Nat Genet. 2015.doi:10.1038/ng.3394.

The first aurochs genome reveals the breeding history of British and European cattle

https://genomebiology.biomedcentral.com/track/pdf/10.1186/s13059-015-0793-z?site=genomebiology.biomedcentral.com

The first aurochs genome reveals the breeding history of British and European cattle

Abstract

Similar works

Full text

Available Versions

Crossref