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Mitochondrial DNA variation reveals maternal origins anddemographic dynamics of Ethiopian indigenous goats

Citation for published version:Tarekegn, G, Tesfaye, K, Mwai, O, Djikeng, A, Dessie, T, Birungi, J, Osama, S, Zergaw, N, Alemu, A,Achieng, G, Tutah, J, Mutai, C, Njuguna, J & Mwacharo, J 2018, 'Mitochondrial DNA variation revealsmaternal origins and demographic dynamics of Ethiopian indigenous goats', Ecology and Evolution, vol. 8,no. 3, pp. 1543-1553. https://doi.org/10.1002/ece3.3710

Digital Object Identifier (DOI):10.1002/ece3.3710

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Ecology and Evolution. 2018;1–11.  | 1www.ecolevol.org

Received:14January2017  |  Revised:30October2017  |  Accepted:10November2017DOI:10.1002/ece3.3710

O R I G I N A L R E S E A R C H

Mitochondrial DNA variation reveals maternal origins and demographic dynamics of Ethiopian indigenous goats

Getinet Mekuriaw Tarekegn1,2,3,4,5  | Kassahun Tesfaye1 |  Okeyo Ally Mwai6 | Appolinaire Djikeng7 | Tadelle Dessie2 | Josephine Birungi4 |  Sarah Osama4 | Netsanet Zergaw2 | Alubel Alemu2 | Gloria Achieng4 | Jack Tutah4 |  Collins Mutai4  | Joyce Njuguna4 | Joram M. Mwacharo8

1DepartmentofMicrobial,CellularandMolecularBiology,AddisAbabaUniversity,AddisAbaba,Ethiopia2InternationalLivestockResearchInstitute(ILRI),AddisAbaba,Ethiopia3DepartmentofAnimalProductionandTechnology,BiotechnologyResearchInstitute,BahirDarUniversity,BahirDar,Ethiopia4BiosciencesEasternandCentralAfrica-InternationalLivestockResearchInstitute(BecA-ILRI)Hub,Nairobi,Kenya5SwedishUniversityofAgriculturalSciences,Uppsala,Sweden6InternationalLivestockResearchInstitute(ILRI),Nairobi,Kenya7CentreforTropicalLivestockGeneticsandHealth,TheUniversityofEdinburgh,Edinburgh,UK8SmallRuminantGeneticsandGenomicsGroup,InternationalCentreforAgriculturalResearchintheDryAreas(ICARDA),AddisAbaba,Ethiopia

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,providedtheoriginalworkisproperlycited.©2018TheAuthors.Ecology and EvolutionpublishedbyJohnWiley&SonsLtd.

CorrespondenceGetinetMekuriawTarekegn,DepartmentofMicrobial,CellularandMolecularBiology,AddisAbabaUniversity,AddisAbaba,Ethiopia.Email:yafetgetinet@gmail.comandJoramM.Mwacharo,SmallRuminantGeneticsandGenomicsGroup,InternationalCentreforAgriculturalResearchintheDryAreas(ICARDA),AddisAbaba,Ethiopia.Email:j.mwacharo@cgiar.org

Funding informationBecA-ILRIHubthroughtheAfricaBiosciencesChallengeFund(ABCF)program;AustralianDepartmentforForeignAffairsandTrade(DFAT)throughtheBecA-CSIRO;SyngentaFoundationforSustainableAgriculture(SFSA);Bill&MelindaGatesFoundation(BMGF);theUKDepartmentforInternationalDevelopment(DFID);SwedishInternationalDevelopmentCooperationAgency(Sida)

AbstractTheHornofAfricaformsoneofthetwomainhistoricalentrypointsofdomesticsintothecontinentandEthiopiaisparticularlyimportantinthisregard.Throughtheanalysis ofmitochondrialDNA (mtDNA)d-loop region in 309 individuals from13populations,werevealthematernalgeneticvariationanddemographicdynamicsofEthiopianindigenousgoats.Atotalof174variablesitesthatgenerated231haplo-typeswereobserved.Theydefinedtwohaplogroupsthatwerepresentinallthe13studypopulations.ReferencehaplotypesfromthesixgloballydefinedgoatmtDNAhaplogroupsshowthetwohaplogroupspresentinEthiopiatobeAandG,theformerbeingthemostpredominant.Althoughbothhaplogroupsarecharacterizedbyanin-creaseineffectivepopulationsizes(Ne)predatingdomestication,theyalsohaveex-periencedadeclineinNeatdifferenttimeperiods,suggestingdifferentdemographichistories.Weobservedsevenhaplotypes,sixweredirectlylinkedtothecentralhap-lotypes of the twohaplogroups andonewas central to haplogroupG. The sevenhaplotypeswerecommonbetweenEthiopia,Kenya,Egypt,andSaudiArabiapopula-tions,suggestingcommonmaternalhistoryandthe introductionofgoats intoEastAfricaviaEgyptandtheArabianPeninsula,respectively.WhileprovidingnewmtDNAdatafromahistoricallyimportantregion,ourresultssuggestextensiveintermixingofgoatsmediatedbyhumansocio-culturalandeconomicinteractions.ThesehaveledtothecoexistenceofthetwohaplogroupsindifferentgeographicregionsinEthiopia

2  |     TAREKEGN ET Al.

1  | INTRODUCTION

Ethiopia ishometomorethan29milliongoats (FAOSTAT,2014;ac-cessedFebruary25,2016),alargenumberofwhichareofindigenoustypeskeptmainlyforsubsistence.Theyinhabitawiderangeofhabitatsandproductionsystemsrangingfromthecoolhighlandstohotaridlow-landenvironments(Abegaz,2014).Basedontheirgeographiclocationandassociatedethniccommunity,Ethiopianindigenousgoatsareclas-sifiedinto13populations(seeDAGRISdatabaseathttp://www.dagris.info/countries/192/breeds?page=2).Thesehavebeenfurthercatego-rized into four family groups based on geographic location, and twoproductionsystemsacross threeagro-ecologicalzones (FARM-Africa,1996).Fromtheanalysisofmicrosatellitemarkers,Tesfaye(2004)re-grouped the13populations into eight types butwith lowbootstrapsupport (<50%). In linewiththe lowbootstrapsupport,STRUCTUREanalysis failed to resolve the eight groups adequately and showed ahighlevelofadmixture.DespitethelackofclarityontheclassificationofEthiopianindigenousgoats,alargegenepoolofautosomalgeneticdiversityoccursinthecountrywhichcanprovidetherawmaterialtosupportbreedingprogramsfortheindigenousstocks.

Globally, at least sixmtDNAd-loop haplogroups (A, B (B1, B2),C,D,F,andG)withaweakphylogeographicstructurehavebeenre-ported in domestic goats (Luikart etal., 2001; Naderi etal., 2007).This was initially interpreted to indicate multiple independent do-mestications(Chen,Su,Wu,Sha,&Zhang,2005;Luikartetal.,2001).However,Naderietal.(2007,2008)suggestedittobetheresultofasingledomesticationcoupledwiththemanagementofwildandsemi-domesticated individuals carrying diversemtDNA lineages followedbygeographicdispersionandsubsequentextinctionofsomelineages.Globally,haplogroupAhasthelargestgeographicdistribution(Pereira,Pereira,Van-Asch,Bradley,&Amorim,2005).HaplogroupBoccursineasternandsouthernAsia,includingMongolia,andatlowfrequenciesinSouthAfricaandNamibia.HaplogroupCoccursatlowfrequenciesin Mongolia, Switzerland, Slovenia, Pakistan, and India, while hap-logroupDoccursonlyinPakistanandIndianlocalgoats.HaplogroupFisexclusivetoSicilywhilehaplogroupGhasbeenobservedinTurkey,Iran,Iraq,SaudiArabia,KenyaandEgypt.

All the six haplogroups occur in thewild ancestor,Capra aega-grus,suggestingthatdomesticationhappenedacrosssouthwestAsia(Naderietal.,2007,2008).Archeologicalfindingsshowthatgoatdo-mestication occurred around 10,500years ago between the ZagrosMountains and the Fertile Crescent (Zeder, 2008; Zeder & Hesse,2000).TheanalysisofmtDNAgenomes (Doroetal.,2014;Nomuraetal.,2013)sidebysidetothatofthed-loopregionshowcongruentclusteringpatternssuggestingacomplexdomesticationprocess.

ArcheologicalevidencehasshownthattheHornofAfrica,andinparticularEthiopia,playedacriticalrole inthehistoryofdispersalofvarious domestic plant and animal species into and out of the con-tinent (Gifford-Gonzalez&Hanotte, 2011;Oliver, 1983). In spite ofthis,majorityofthestudiesperformedsofaronindigenousgoats,havelacked samples from the region.On theother hand,various studieshave shown that socio-anthropological (humanmovements, culturalexchanges,war,etc.)andnatural (droughts, floods,etc.)eventshavecontributed to the geographic dispersion and intermixing of differ-entlivestockspecies(Girma,1988;Yilma,1967)andtheymighthaveshaped the genetic landscape of indigenous domestic stocks in theregion.Inthisstudy,weanalyzedmtDNAd-loopsequencestoinvesti-gatethewithinandbetweenpopulationmaternalgeneticvariationanddiversity,anddemographicdynamicsofindigenousgoatsinEthiopia.

2  | MATERIALS AND METHODS

2.1 | Sampling and DNA extraction

Atotalof309bloodsamples representing13Ethiopian indigenousgoatpopulationsweresampledfromfarmer’sflocksandusedforthestudy.Duringsampling,alleffortsweremadetoavoidcloselyrelatedindividuals.GenomicDNAwasextractedfromthebloodsamplesfol-lowingShinde,Gujar,Patil,Satpute,andKashid(2008).

2.2 | PCR amplification and sequencing

The entire mtDNA d-loop region (1,061bp) was amplified usingnestedPCR(TableS1).ThePCRreactionswerecarriedout in20-μl reactionvolumesmadeupoftheAccuPower®PCRPremix(Bioneer-Daejeon, Korea), 0.2μM of each primer, 1.5% Hi-Di™ formamide(Applied Biosystems, USA), 0.005mg of Bovine Serum Albumin(ThermoScientific),and50ngoftemplateDNA.Atwo-stagetouch-downPCRinvolvinganinitialdenaturationat95°Cfor3minfollowedbythefirststageofamplificationoffivecycles(denaturationat90°Cfor10s,annealingat58°Cfor40s,andextensionat72°Cfor30s),anda secondstage that involved thesameprofilebut30cyclesofamplificationandanannealingtemperatureof53°C,wasperformed.Afinalextensionstepat72°Cfor7mincompletedthePCR.ThePCRproducts were purified using the QIAquick® PCR Purification Kit(Qiagen,HildenGermany)followingthemanufacturer’s instructions.ThepurifiedproductsweresequencedusingtheBigDyeTerminatorv3.1CycleSequencingChemistry (AppliedBiosystems)andtheABIPrism 3130XL automatic capillary sequencer (Applied Biosystems,USA)followingthemanufacturersprotocols.

resulting in a large caprine genetic diversity that can be exploited for geneticimprovement.

K E Y W O R D S

Bayesianskylineplot,geneticdiversity,haplogroups,haplotypes,populationexpansion

     |  3TAREKEGN ET Al.

2.3 | Data analysis

Forall theanalysesundertakenhere,thedefaultvaluesandparam-eters inherent in thealgorithmsandsoftware’swereusedandonlydeviations from thedefault arementioned.Prior toanalysis, all thechromatogramswerevisualizedwiththeCLCWorkbench7.0.4(CLCBio-Qiagen). The sequence fragments were edited manually usingMEGA6(Tamura,Stecher,Peterson,Filipski,&Kumar,2013)tocor-rectpossiblebasecallingerrors.MultiplesequencealignmentswereperformedusingClustalOmega(Sieversetal.,2011),andvariablesiteswere scored against theC. hircus reference sequence (Genbank ac-cessionnumberGU223571).Wegenerated309sequencesandde-terminedthehaplotypeswithDnaSPv5(Librado&Rozas,2009).Thelevelof geneticdiversity, determinedas thenumberofhaplotypes,haplotypediversity,nucleotidediversity,andmeannumberofnucleo-tide differences between haplotypes and their standard deviations,werecomputedforeachpopulationandacrossallpopulationsusingArlequin3.5(Excoffier&Lischer,2010).

Tovisualizethegeneticrelationshipbetweenindividualsandpop-ulations,aphylogenetictreewasconstructedusingallthehaplotypesgeneratedinEthiopiangoatswiththeneighbor-joining(NJ)algorithmimplementedinMEGA6.Thelevelofconfidenceassociatedwitheachbifurcationwasevaluatedwith1,000bootstrapreplications.ToobtainfurtherinsightsintothegeneticrelationshipsbetweenthehaplotypesanddeterminethenumberofdistinctmtDNAd-loophaplogroupspres-entinthedataset,themedian-joining(MJ)network(Bandelt,Forster,&Röhl,1999)wasconstructedusingNetworkv4.6(www.fluxus-en-gineering.com).Allthemutationsandcharacterstateswereweightedequally.TovisualizethevariationinEthiopiangoatsinthecontextofthe global caprinediversity, 229 sequencesof domestic goats from20countriesandrepresentingthesixgloballydefinedmtDNAd-loophaplogroups(Naderietal.,2007,2008)andfourhaplotypesofC. ae-gagrus (Genbank accession numberAJ317864–AJ317867)were re-trievedfromtheGenbank(TableS2)andincludedintheNJtreeandMJnetworkanalysis.Asthereferencehaplotypesrepresentingthesixhaplogroupsaredefinedbasedonthevariationinthefirsthypervari-ableregion (481bp)ofthed-loop (Luikartetal.,2001;Naderietal.,2007,2008),thehaplotypesgenerated inEthiopiangoatswerefirsttruncatedto481bpandthenusedintheconstructionoftheNJtreeandMJnetwork.TheHVI regioncorresponds topositions15,709–16,190bpoftheC. hircusmtDNAreferencesequence(Genbankac-cessionnumberGU295658).

To partition genetic variation among populations and groups ofpopulations, analysis ofmolecularvariance (AMOVA)was performedfollowing1,000permutationsinArlequinv3.5.TheanalysiswaslimitedtoEthiopiangoatsandvarioushierarchicalclustersweretestedviz(i)as-sumingnoclustersinthedataset,(ii)betweenthethreegroupsofpop-ulationsasdefinedbyFARM-Africa(1996),and(iii)betweenpopulationgroupings revealedby theNJ treeandMJnetwork.Phi (ϕ) statisticsrepresentinghaplotypecorrelationsatvarioushierarchical levels (ϕCT,ϕSC,ϕST)were calculated. Levels of significanceof thevariance com-ponentsassociatedwiththehierarchicalclusterswereevaluatedwith1,000nonparametricbootstrapcoalescentsimulationsinArlequinv3.5.

Thehistoricaldynamicsanddemographicprofilesofeachpopu-lationandhaplogroupwereinferredfrommismatchdistributionpat-terns(Rogers&Harpending,1992).Thechi-squaretestofgoodnessoffitandHarpending’sraggednessindex“r”(Harpending,1994)sta-tisticswereusedtoevaluatethesignificanceofthedeviationsoftheobservedsumofsquaresdifferences(SSD)fromthesimulatedmodelofexpansion(demographicorspatial)following1,000coalescentsim-ulations.Tocomplementthemismatchdistributions,Fu’sFS(Fu,1997)andTajima’sD(Tajima,1989)statisticswerealsocalculatedusingtheinfinitesitesmodelinArlequinv3.5.

The demographic dynamics and history of Ethiopian goat pop-ulations were further investigated by generating Bayesian SkylinePlots(BSPs;Drummond,Rambaut,Shapiro,&Pybus,2005)usingthepiecewiseconstantfunctionimplementedinBEAST2.0(Drummond,Suchard,Xie,&Rambaut,2012) followingSalim,Taha,Hanotte,andMwacharo(2014).Inbrief,theHKY+GnucleotidesubstitutionmodelwasusedfortheanalysisandeachMarkovChainMonteCarlosimula-tion(MCMC)runswereperformedfor20milliongenerationsthatweresampledevery1,000generations.Theinitialtwomilliongenerationsservedasburn-in.ConvergenceoftheposteriorestimatesoftheNetothelikelihoodstationarydistributionwasevaluatedwithTRACERv1.6(http://tree.bio.ed.ac.uk/software/treestat/).ThisanalysiswaslimitedtoEthiopiangoatsandthe481bpHVIofthemtDNAd-loopregion.WecalibratedtheBSPsusingthemolecularrateofevolution(μ)oftheHV-IregioningoatmtDNAd-loopof2.73×10−7substitutions/site/year(s/s/yr)followingNomuraetal.(2013).

3  | RESULTS

3.1 | mtDNA sequence variation and genetic diversity

Threehundredandninesequencesspanningtheentire1,061bpofthecaprinemtDNAd-loopweregenerated.ThesequenceshavebeendepositedwiththeGeneBankunderaccessionnumbersKY747687–KY747993. Following their alignment against the caprine referencesequence(AccessionNo:GU223571),174variablesites(165transi-tions,sixtransversions,andthreeInDels)wereobserved.Thesede-fined231haplotypes (Table1)ofwhich22weresharedbyat leasttwopopulations(TableS3).Allthe13populationsshowedhighlev-elsofmaternalgeneticdiversity(Table1).Thenumberofhaplotypesrangedbetween12 (inAgew) and30 (inAfar). The lowest level ofhaplotypediversity(0.9500±0.037)wasobservedinKeffawhilethehighest (1.0000±0.020) was observed in the Short-eared Somali,HarargheHighland,andWoyto-Guji.Thenucleotidediversityrangedfrom0.0143±0.0019inAfarto0.0180±0.001inAbergelle.

3.2 | Population phylogenetic analysis

Weused theHV-I (481bp) sequences of Ethiopian goats and 229HV-IhaplotypesretrievedfromtheGeneBankandrepresentingthesixmainhaplogroupsobservedingoatstoconstructaNJtreetoas-sessgenetic relationships.TheNJtreerevealedthreewell-resolved

4  |     TAREKEGN ET Al.

clusters;twowerespecifictoEthiopianindigenousgoatsandthethirdone clustered together the haplotypes representing haplogroupsB,C,D,F,andwildcapras(Figure1).ToobtainfurtherinsightsintothephylogeneticrelationshipsandputtheEthiopiangoatsinthecontextof caprine global diversity,we included in the dataset used forNJanalysis,sequencesfromEgyptian,SaudiArabia, Iran,Iraq,Pakistan,andNigeriagoatsandgeneratedtheMJnetwork.Asexpected, theanalysis also revealed two clusters in Ethiopian goats which wereseparatedby10mutations (Figure2).Both theNJ treeand theMJnetworkrevealedthetwoclustersinEthiopiangoatswerepartoftheglobally observedhaplogroupsA andG (Figure2).HaplogroupA isthemostcommonand included185haplotypes (80.1%of thetotalnumberofhaplotypes)whilehaplogroupGcomprised46haplotypes(19.9%).Noneofthetwohaplogroupswasexclusivetoasinglepopu-lation,geographicregion,orproductionsystem(FigureS1).Wealsoobserved137medianvectorsontheMJnetwork.

3.3 | Population genetic structure

AMOVA analysis incorporating the 13 populations assuming no hi-erarchicalclusters,aswellas,thethreegroupsproposedbyFARM-Africa(1996)showedthat97%ofthetotalgeneticvariationpresentin Ethiopian indigenous goats occurredwithin individuals, less than2%of the variationwasdue to genetic differencesbetweenpopu-lations and less than1% could be explained by genetic differencesbetweengroupsofpopulations(Table2).PerformingAMOVAtakingintoaccounttheresultsoftheNJtreeandMJnetworkrevealedthat

59.11%ofthegeneticvariationoccurredwithinthetwohaplogroups,while40.89%wasexplainedbygeneticdifferencesbetweenhaplo-groupsAandG(Table2).

3.4 | Population and historical demographic dynamics

Weassessedmismatchdistributionpatterns,foreachpopulationandfor the two haplogroups revealed by theNJ tree andMJ network(Figure3),toelucidatethedemographicdynamicsofEthiopianindig-enousgoats.ThemismatchdistributionpatternsforeachpopulationwerebimodalandtheobservedpatterndidnotdeviatesignificantlyfromthatexpectedunderanullhypothesismodelofeitherspatialordemographicexpansionexceptforAbergelle(Table3).ThevariationsaroundthecurveswerealsonotsignificantexceptforAgew(Table3).Abimodalpatternofmismatchdistributions,withtheobservedpat-ternnotdeviatingsignificantlyfromtheexpected,wasalsoobservedfortheglobaldatasetincorporatingthe13Ethiopianpopulationsandthe twohaplogroups, respectively (Figure3 andTable3). These re-sultsweresupportedbyTajima’sDandFu’sFSstatistics;bothwerenegative and significant for each population,with the exception ofAbergelleandGondarwhoseTajima’sDwasnegativebutnotsignifi-cant,fortheglobaldatasetof13populations,andforthetwohap-logroups.Thebimodalpeaksobservedinthetwohaplogroupsweresurprisingandunexpected.Wethereforecountercheckedallthese-quencesagainsttheir respectivechromatogramsforbasecallinger-rors.Thesequencesturnedouttobecorrectandtherewasnomix-up

TABLE  1 Maternalgeneticdiversityof13EthiopiangoatpopulationsfromtheanalysisoftheHV-IregionofthemtDNAd-loop

Population N S H Hd ± SD π ± SD K

No. of haplotypes (%)

Haplogroup A Haplogroup G

Short-earedSomali 17 66 17 1.0000±0.020 0.0158±0.002 16.692 14(82.35) 3(17.65)

Long-earedSomali 19 65 17 0.9883±0.021 0.0159±0.002 16.866 14(82.35) 3(17.65)

Nubian 37 88 25 0.9728±0.013 0.0155±0.001 16.378 21(84.00) 4(16.00)

HarargheHighland 22 65 22 1.0000±0.014 0.0165±0.002 17.446 21(71.43) 6(28.57)

Abergelle 35 78 29 0.9882±0.010 0.0180±0.001 19.005 21(72.41) 8(27.59)

Arsi-Bale 20 69 18 0.9895±0.019 0.0131±0.002 13.848 16(88.89) 2(11.11)

Ambo 16 68 13 0.9667±0.036 0.0170±0.003 17.992 13(84.62) 2(15.28)

Afar 33 80 30 0.9943±0.009 0.0143±0.002 15.125 24(80.00) 6(20.00)

Agew 15 56 12 0.9714±0.033 0.0144±0.002 15.181 11(91.67) 1(8.33)

Gumez 25 66 19 0.9667±0.024 0.0163±0.002 17.220 14(77.78) 4(22.22)

Gondar 27 70 24 0.9886±0.015 0.0176±0.001 18.621 15(65.22) 8(34.78)

Keffa 25 62 20 0.9500±0.037 0.0093±0.002 9.853 19(90.48) 2(9.52)

Woyto-Guji 18 63 18 1.0000±0.019 0.0164±0.002 17.353 14(77.78) 4(22.22)

Overall 309 174 231 0.9967±0.001 0.0158±0.001 17.427 – –

HaplogroupA 248 154 185 0.9957±0.025 0.0098±0.001 10.344 – –

HaplogroupG 61 69 46 0.9831±0.018 0.0057±0.002 6.006 – –

N,samplesize;S,numberofpolymorphicsites;H,numberofhaplotypes;Hd,haplotypediversity;π,nucleotidediversity;K,averagenumberofnucleotidedifferences;SD,standarddeviation.

     |  5TAREKEGN ET Al.

between the sequencesused to generate thedatasets for themis-matchdistributionanalysis.ThebimodalpeaksalsoappearnottobeauniquefeatureofhaplogroupsAandGinEthiopiangoats.Wealso

observedtwopeaks inhaplogroupA inSudanesegoats.Chenetal.(2005)observedabimodalpeakforHaplogroupB inChinesegoatsand the dataset of Kibegwa,Githui, Jung’a, Badamana, andNyamu

F IGURE  1 Neighbor-joiningtreeconstructedusingtheHV-IregionofthemtDNAd-loopof13Ethiopiangoatpopulationsincludingreferencehaplotypesrepresentingsixhaplogroupsobservedingoatsandtwowildancestorsanalyzedinthisstudy

F IGURE  2 Median-joiningnetworkbasedontheanalysisof481bpoftheHV-Iinvolvingthe231haplotypesobservedin13EthiopiangoatpopulationsandreferencehaplotypesrepresentingsixmtDNAhaplogroupsanalyzedinthisstudy.Countryoforiginofthereferencehaplotypesandtheirorigin.HaplogroupA(India,Italy,France,Jordan,Iran(N=2);Naderietal.,2007);HaplogroupB(Laos(Mannen,Nagata,&Tsuji,2001),Azerbaijan(Naderietal.,2007),Mongolia(Luikartetal.,2001)andChina(Liuetal.,2006));HaplogroupC(India(Joshietal.,2004),Swizerland(Luikartetal.,2001),Spain(Naderietal.,2007),China(Liuetal.,2006));HaplogroupD(India(Joshietal.,2004),Austria(Naderietal.,2007),China(Liuetal.,2005));HaplogroupF(Sicily:Sardinaetal.,2006);HaplogroupG(Iran,TurkeyandEgypt(Naderietal.,2007))

6  |     TAREKEGN ET Al.

(2015)appearsalsotoshowbimodalpeaksforhaplogroupsAandGinKenyangoats.Takentogether,theseresultssuggesteitheraspa-tialand/ordemographicexpansionfortheEthiopianindigenousgoatsandthetwohaplogroups,respectively.

To obtain a better resolution of the demographic history andprofile of Ethiopian goats, we modeled changes in maternal effec-tivepopulationsizes (Ne)over timebygeneratingBSP’s for thetwohaplogroups(Figure4a,b).TheyrevealanincreaseinNefromaround55,000and21,500YBPforhaplogroupsAandG, respectively.ThisincreaseisfollowedbyagradualdeclineinNefromaround5,000and1,500YBPwhichcontinuestodate,foreachhaplogroup,respectively.

4  | DISCUSSION

Althoughevidence indicatesthat theHornofAfricawasagatewayfor various domesticates into the African continent (Hassan, 2000;Newman,1995;Wetterstrom,1993), thedemographicdynamicsofindigenousgoats intheregionremainpoorly investigated.Here,weanalyzedthesequencevariationof themtDNAd-loopregionof13populations of Ethiopian indigenous goats to assess their maternalorigin, genetic differentiation, and demographic historical profiles.Theresultsrevealed231haplotypesfromtheanalysisof309mtDNAd-loop sequences which gave an average haplotype diversity of0.997±0.001 (range0.950±0.037 to1.000±0.020).This averagevalueissimilartothatofIberian(0.996)andEuropean(0.994)goatsbut itshigherthanthatofSicilian (0.806–0.969),SouthandCentralAmerican (0.963), Atlantic (0.965; Amills etal., 2008), and Kenyan

goats (0.981±0.006;Kibegwaetal.,2015).TheseresultssuggestahighlevelofmaternalgeneticvariationinEthiopianindigenousgoatsthat have arisen from past and recent population intermixing. Thisintermixinghasprovidedabroadrangeofgeneticdiversitythatcanbeexploitedinthedesignofgeneticimprovementandconservationprograms.Theresultalsosuggeststhatthematernalgeneticdiversityoftheindigenousgoatsisnotunderimminentdangeroflossthroughextinctionordilutionthroughcrossbreedingwithexoticsbreedsandintheeventthatonepopulationislost,itispossibletoreconstituteitfromtheothers.

To portray the genetic relationships among Ethiopian goats,weusedthe231haplotypestoconstructaNJtree(Figure1)andMJnet-work (Figure2).Theclusteringpattern revealed twowell-supportedhaplogroups with no phylogeographic structure. The incorporationof reference haplotypes revealed them to be haplogroupsA andG(Naderietal.,2007,2008).AMOVAshowedthatthetwohaplogroupsaccountedfor40.89%ofthematernalgeneticvariationinEthiopiangoats.Thisprovidesfurthersupportforthegeneticdistinctionofthetwohaplogroupsandsuggestingtheintroductionandpresenceofatleasttwodistinctgeneticgroupsofgoats intheHornofAfrica.Thetwo haplogroups could have been introduced from different geo-graphic domestication areas as Nomura etal. (2013) showed thattheirdivergenceoccurredprior todomestication.Wealsoobservedahighnumberofmedianvectors(n=137)exceedingthoseobservedinotherpopulations(Amillsetal.,2008;Chenetal.,2005;Joshietal.,2004;Luikartetal.,2001;Naderietal.,2007,2008;Sultana,Mannen,& Tsuji, 2003). This large number of median vectors may likely bean inherent feature of the Ethiopian indigenous goats because we

TABLE  2 ResultsofAMOVAbasedontheanalysisoftheHV-IregionofthemtDNAd-loopin13Ethiopiangoatpopulations

Grouping Source of variation Degrees of freedom Variance componentsPercentage of variation

Allpopulations Amonggroups 12 0.220 2.63

Withinindividuals 294 8.166 97.37

Total 306 8.386

Agro-ecology Amonggroups 2 0.061 0.73

Amongpopulationswithingroups 10 0.177 2.11

Withinindividuals 294 8.166 97.16

Total 306

Productionsystem Amonggroups 1 0.027 0.33

Amongpopulationswithingroups 11 0.208 2.48

Withinindividuals 294 8.166 97.19

Total 306 8.402

Goatfamily Amongfamilygroups 3 0.030 0.37

Amongpopulationswithinfamilygroups

9 0.196 2.34

Withinindividuals 294 8.171 97.29

Total 306 8.398

Basedonhaplogroups Amonghaplogroups 1 4.881 40.89

Withinhaplogroups 305 7.055 59.11

Total 306 11.936

     |  7TAREKEGN ET Al.

observedalargenumberofnodes(n=192)andedges(n=335)thatrepresent subpopulations and population subdivisions, respectively(Huson&Bryant,2006) in aphylogenetic tree thatweconstructedforthe13populationsusingautosomalSNPmarkers(MekuriawGM,LiuB,OsamaS,ZhangW,TesfayeK,DessieT,MwaiAM,DjikengA,Mwacharo JM “unpublished data”). These results demonstrate notonly the presence of high genetic variation in Ethiopian indigenousgoatsbutalsoa likelycomplexmaternalgenetichistory.The lackofphylogeographic structure appears to be a common feature of do-mestic goats; it has been observed in aworldwide dataset (Luikartetal., 2001; Naderi etal., 2007, 2008), in the Indian subcontinent(Joshietal.,2004;Sultanaetal.,2003)andChina(Chenetal.,2005).Theeaseoftransportinggoats,theiruseasitemsoftradeandsocio-culturalexchange(tostrengthenfriendshipandfamilybonds/ties),and

their inherent ability to adapt to a diverse rangeof production andecologicalenvironments,relativetoforinstancecattle,hasbeenusedto explain their lack of phylogeographic structure and high level ofgeneticdiversity.

HaplogroupAisthemostdiverseandhasthewidestgeographicdistributionacrossEthiopiaandtheworld(Naderietal.,2007,2008).Naderietal.(2008)suggestedthatitoriginatedfromEasternAnatolia.HaplogroupGhas beenobserved inTurkey, Iran, SaudiArabia, andEgyptandNaderietal. (2007)suggestedthat itoriginatesfromIran(Northern and Central Zagros). Both haplogroups (A and G) havebeen observed in Egypt (Naderi etal., 2007), one of the historicalentrypointsofdomesticatesintotheAfricancontinent,andrecentlyinKenya(Kibegwaetal.,2015).GiventhattheearliestarcheologicalevidenceforthepresenceofdomesticgoatsinAfricadatesto5000

F IGURE  3 Mismatchdistributionpatternsforeachandacrossthe13EthiopiangoatpopulationsanalyzedinthisstudyandforthetwohaplogroupsrevealedbytheNJtreeandMJnetworkanalysis

8  |     TAREKEGN ET Al.

BCinNorthAfrica,that is,Egypt,Libya,andAlgeria (Hassan,2000),it is likelythatthetwohaplogroupsarrivedattheirearliest inEgyptfollowingterrestrialroutescrisscrossingtheSinaiPeninsula,RedSeaHills, andMediterranean Sea Coast (Hassan, 2000). Following theirarrival inEgypt,archeologicalevidence indicates that, togetherwithsheep,goatsdispersedsouthwardsintoSudanandEthiopiafollowingtheNileriverbasin(Chaix&Grant,1987;Clutton-Brock,2000).Thefactthatweobservedtwohaplotypes(H128andH133)ofhaplogroupAthataresharedbetweenEthiopianandEgyptiangoats,two(H164andH166)sharedbetweenEthiopiaandKenyangoatsandone(H102)sharedbetweenEthiopianandSaudiArabiangoats(Figure2andTableS4), suggest that the southwardmovement of goats along theNilevalley,aswellas,themovementofgoatsacrosstheRedSeafromtheArabian Peninsula could have introduced haplogroupA to Ethiopia.The Ethiopian and Kenyan goats also shared the central haplotype(H13)ofhaplogroupGwithSaudiArabiangoatssuggestingapossibleintroductionofthishaplogrouptoEthiopia,eitherindependentlyorasacompaniontohaplogroupA,fromtheArabianPeninsula.Indeed,theprehistoricandhistorictranslocationofdomesticatesincludingcattle,sheep,andgoatsbetweentheArabianPeninsula,northeastAfrica,andtheHornofAfricafollowingterrestrialandmaritimerouteshasbeenreported (see review by Boivin & Fuller, 2009). Similarly, Ethiopiangoats share four haplotypes (two each of haplogroupA (H164 andH166) andG (H13 andH125))withKenyan goats suggestingmostlikelycommonmaternaloriginsanddispersionpatternsofgoatsfoundinthewiderHornofAfricaregion.

We observed a bimodal pattern of distribution ofmismatches ineach,andacrossthe13populations,ofEthiopianindigenousgoats.Thisresultappearstosuggestthelikelyexpansionofthetwohaplogroups

into Ethiopia as they are found in each of the populations analyzed.However,thismaynotbethecase.Aseparateanalysisofthetwohap-logroupsalsorevealedthebimodalpattern,suggestingtheexistenceoflargevariationwithinthehaplogroups.Collietal.(2015)foundatleastsevensubhaplogroups (A1–A7)withinhaplogroupA.Althoughnotasdistinctasweobserveinourdataset,thedataofKibegwaetal.(2015)alsoappeartoshowbimodalpeaksforhaplogroupsAandGinKenyangoatsandChenetal.(2005)alsoobservedabimodalpeakforhaplogoupBinChinesegoats.Furthermore,theBSPanalysisinterestinglyindicatesthattheexpansionofthetwohaplogroupspredatesthetimeperiodofgoatdomestication,afindingthatwasalsoreportedbyNomuraetal.(2013)andCollietal. (2015).Their introductionalone intoEthiopia isthereforenot sufficient toexplain thebimodalpatterns.Toouropin-ion, an alternative interpretationwould be that the bimodal patternsindicate, in general, two independent expansion events of goats intoEthiopiaand,mostlikely,thewiderHornofAfricaregion.Theexpansiondepictedbythefirstpeakcouldcorrespondtothe initial introductionofgoatstotheregionfromeitherEgyptand/ortheArabianPeninsulaandthesecondpeakcouldrepresentthesecondarydispersalofgoats,throughtradeandsocio-culturalinteractions,withinandacrossEthiopiaandtheregionatlarge.Thissecondarydispersalmostlikelycontributedto the geographic inter-mixing of the two haplogroups. Indeed, mo-leculargeneticevidencehasrevealedtheabsenceofphylogeographicstructure among Ethiopian ethnic communities (Christopher, 2011;Paganietal.,2012)andindigenouscattlepopulations(Dadietal.,2008;Edeaetal.,2013).Thishasbeenattributedtopastandrecentextensivehumanmovementsassupportedbyhistorical,social,andanthropolog-icalevidences(Habitamu,2014;Mpofu,2002;Yilma,1967).TheBSPsrevealedareductioninNebeginningaround5,000and1,500YBPfor

TABLE  3 PopulationdemographicparametersestimatedfromtheanalysisoftheHV-IregionofthemtDNAd-loopin13Ethiopiangoatpopulations

Population/haplogroup N S SSD (p-value)Raggedness index “r” (p- value)

Tajima’s D (p-value)

Fu’s FS (p-value)

Short-earedSomali 17 66 0.02(.14) 0.01(.74) −0.61(.28) −6.31(.01)

Long-earedSomali 19 67 0.02(.12) 0.01(.74) −0.67(.27) −3.8(.07)

HarargheHighland 22 65 0.03(.12) 0.02(.11) −0.09(.56) −9.77(.00)

Nubian 37 88 0.01(.08) 0.01(.23) −0.82(.22) −3.95(.11)

Abergelle 35 78 0.02(.04) 0.01(.64) 0.01(.60) −12.32(.00)

Arsi-Bale 19 69 0.01(.53) 0.01(.82) −1.16(.12) −6.22(.01)

Ambo 16 68 0.03(.09) 0.02(.51) −0.52(.32) −0.73(.31)

Afar 33 80 0.02(.22) 0.01(.86) −0.87(.20) −15.69(.00)

Agew 15 56 0.03(.13) 0.06(.04) −0.51(.2) −1.86(.15)

Gumez 25 66 0.02(.28) 0.01(.46) −0.06(.51) −3.06(.11)

Gondar 27 70 0.02(.13) 0.01(.50) 0.10(.58) −6.39(.02)

Keffa 24 62 0.01(.40) 0.01(.63) 1.574(.03) −5.55(.02)

Woyto-Guji 18 63 0.02(.37) 0.01(.89) −0.22(.47) −6.8(.01)

HaplogroupA 258 164 0.001(.23) 0.01(.31) −1.50(.02) −24.99(.00)

HaplogroupG 49 89 0.0002(.97) 0.03(.79) −1.86(.01) −26.31(.00)

All 309 174 0.02(.20) 0.02(.55) −1.53(.05) −25.63(.00)

N,samplesizes;S,segregatingsites;SSD,sumofsquareddeviations.

     |  9TAREKEGN ET Al.

haplogroupAandG,respectivelysuggestingdifferentdemographichis-toriesforthetwohaplogroups.Thetimingofthiseventseemstosug-gestthatthedeclineinNeforhaplogroupAstartedpriortoitsarrivalinEthiopiawhilethatofhaplogroupGstartedwhenithadalreadyarrivedinthecountry.WhilethedeclineinhaplogroupAcanbeattributedtothebottleneckcreatedbytheintroductionofasmallnumberofindivid-ualsoftheoriginalgeneticstock(Bruford,Bradley,&Luikart,2003),thatofhaplogroupGmayhavebeendrivenbytherinderpestpandemicofthe1800s(Blench,1993;Payne&Hodges,1997)andasequelofseveredroughtsandpoliticalupheavals(Verschuren,Laird,&Cumming,2000)thatoccurredinthewiderHornofAfricaregion.ThelattercouldalsohaveaffectedhaplogroupA.AsimilardeclineinNedatingtothesametimeperiodhasalsobeenobservedintheEastAfricanshorthornzebucattle fromwestern Kenya using SNP genotype data (Mbole-Kariukietal.,2014).

5  | CONCLUSIONS

WeobservedahighlevelofmaternalgeneticdiversityinEthiopiangoatpopulationswhichwasexplainedby231haplotypes thatde-finedtwohaplogroups(AandG)thatlackedaclearphylogeographicstructure.Asobservedinotherpopulations,haplogroupAwasthe

most diverse and geographically widespread. Human-mediatedtranslocationsthroughcommercialtrading,socio-culturalexchanges,and seasonal migrations in search of forage and water resourcescould explain the lackof phylogeographic structure. The initial in-troductionof the twohaplogroupsand their subsequent intermix-inghascreatedagenetictreasure-troveofcaprinegeneticdiversitythatcanbeexploitedinbreedingprogramsaimedatimprovingthespecies.

ACKNOWLEDGMENTS

We extend special thanks to flock owners and the district agricul-ture and rural development offices in Ethiopia for support duringsampling.ThisprojectwassupportedbytheBecA-ILRIHubthroughthe Africa Biosciences Challenge Fund (ABCF) program. The ABCFProgramisfundedbytheAustralianDepartmentforForeignAffairsandTrade(DFAT)throughtheBecA-CSIROpartnership;theSyngentaFoundation for Sustainable Agriculture (SFSA); the Bill & MelindaGates Foundation (BMGF); the UK Department for InternationalDevelopment (DFID); and the Swedish International DevelopmentCooperation Agency (Sida). JMM was supported by the CGIARResearchprogramonLivestock(LivestockCRP)andILRIandICARDAthankthedonorssupportingtheLivestockCRP.Thisstudyformspart

F IGURE  4 BayesianSkylinePlotsfor(a)HaplogroupAand(b)HaplogroupGbasedontheanalysisoffirst481bpoftheHV-IregionofmtDNAd-loop

10  |     TAREKEGN ET Al.

ofourongoingeffortstounderstandlocalindigenouslivestocktoim-provetheirproductivity.

CONFLICT OF INTEREST

Nonedeclared.

AUTHOR CONTRIBUTIONS

KT,OAM,AD,TD,andJBconceivedthestudy.GMdidthesampling;OAM,AD,TD,andJBprovidedguidanceduringsamplingandlabora-toryanalysis;GM,SO,NZ,AA,GA,JT,CM,andJNperformedlabo-ratoryanalysis anddatamanagement.GManalyzed thedata; JMMguideddataanalysisandinterpretation;GMandJMMwrotetheman-uscript.Allauthorsreadandapprovedthefinalmanuscript.

ETHICAL CLEARANCE

All theanimalsused in thisstudyareownedbysmall-scale farmersandpastoralists inEthiopia.Prior tosampling, theobjectivesof thestudywerecommunicatedtoallthefarmers,intheirlocallanguagesforeaseofunderstanding,followingwhichpermissionwasobtainedtosampletheanimals.

ORCID

Getinet Mekuriaw Tarekegn http://orcid.org/0000-0001-7221-2473

Collins Mutai http://orcid.org/0000-0002-0951-9023

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How to cite this article:TarekegnGM,TesfayeK,MwaiOA,etal.MitochondrialDNAvariationrevealsmaternaloriginsanddemographicdynamicsofEthiopianindigenousgoats.Ecol Evol. 2018;00:1–11. https://doi.org/10.1002/ece3.3710