Whole-genome Resequencing Reveals World-wide Ancestry And Adaptive Introgression Events Of Domesticated Cattle In East Asia

The domestication of cattle from aurochs(Bos primigenius)was one of the most significant achievements of the Neolithic period.By supplying meat,leather,and draught force for ploughing and transportation,cattle became the most important livestock in East Asian agricultural society.Nowday,cattle are still an important domesticated animal resource in East Asia.Modern cattle breeds probably descended from multiple domestication events of wild aurochs in different geographic areas ~10,500 years before present(YBP).Two primary domestication centre in the Near East and the Indus Valley resulted in humpless taurine(Bos taurus)and humped indicine(Bos indicus)cattle,respectively.Population analyses based on genomic single nucleotide polymorphism(SNP)array data revealed three major groups of cattle,including Eurasian taurine,African taurine,and Asian indicine.East Asian domestic cattle share origins with other taurine and indicine backgrounds.Archaeological evidence suggested that B.taurus may have been imported into East Asia from the Fertile Crescent during the late Neolithic period(between 5,000 and 4,000 YBP)and B.indicus may have dispersed from the Indian subcontinent to East Asia at a later stage,from 3,500 to 2,500 YBP,which led the hybridization between taurine and indicine cattle in Central China.East Asia is rich in bovine resources with fifty-three indigenous cattle breeds in China.Several bovine species including yak,gayal,gaur and banteng were also observed in China and adjacent regions,and hybridization of these species occurs worldwide.All these events contributed to the complex histories of East Asian cattle.The analysis of origin of East Asian cattle were based on Y-SNP markers,segments of mtDNA and genomic SNP array data,however,the whole-genome diversity of East Asian cattle has not been explored in depth.In this study,through analyzing the whole genome re-sequencing data of 49 modern breeds and eight North Chinese ancient samples form Shimao sites,this project will reveal the genetic variations and germplasm characteristics of autosome,Y-chromosome and mitochondrial genome of Chinese local cattle,investigate the origin and evolution,population history dynamics,gene flow,and migration events,clarify the historic introgression time and proportion between Chinese cattle and related Bovini species.Our main results are as follow:1.Autosomal and Y chromosomal variants revealed three types of ancestry of East Asian cattleFive geographically distributed ancestral components were observed and labelled based on autosomal(Y-chromosome)evidence: European taurine with the paternal lineage Y1,Eurasian taurine with Y2 a,East Asian taurine with Y2 b,Chinese indicine with Y3 a,and Indian indicine with Y3 b.European taurine ancestry(Y1)was mainly observed in West European breeds.Eurasian taurine ancestry(Y2a)was identified at the highest frequency in both CentralSouth European breeds and Northwest Chinese breeds.Tibetan and Northeast Asian breeds from two separate geographical regions formed a distinct East Asian taurine group(Y2b).Within B.indicus,Chinese indicine cattle(Y3a)were clearly separated from Indian indicine(Y3b)cattle.The Chinese indicine ancestry was observed at the highest frequency in South China and progressively decreased northward.We find that East Asian cattle populations are mainly composed of three distinct types of ancestry and paternal lineages,including a specific East Asian taurine ancestry(Y2b),a Eurasian taurine ancestry(Y2a)shared with European breeds,and a new type of Chinese indicine(Y3a)that significantly different from Indian indicine.2.The relationship between ancient Shimao and modern cattle revealed the multiple migrations of cattle in East AsiaAncient evidence showed that the samples in the late Neolithic Shimao site in northern China(3,975–3,835 cal BP)had the closest affinity with East Asian cattle.Combined with the geographical distribution of Y haplogroups,this finding suggests that at least two migration phases might have occurred in the history of East Asian B.taurus.We speculate that the earliest cattle population(East Asian taurine)might be introduced before ~3,900 YBP.Later on,the East Asian taurine cattle might become widespread all over northern China and margins of the Tibetan Plateau.The earlier strand may have migrated from Northeast China to Japan via the Korean peninsula.The Eurasian strand(Y2a)possibly was introduced and spread later by the expansion of early pastoralism,leading to west-to-east immigrations,which led to gene flow across eastern Eurasia and partial replacement of East Asian taurine ancestry(and the Y2 b lineage)in northern China.3.Extensive gene flow between East Asian cattle and bovine speciesThe proportion of the Chinese indicine genome inferred to be of banteng ancestry is 2.93% per genome,which led to the unique genomic diversity of Chinese indicine cattle.The estimated introgression time was ~2.9 thousand years ago(kya).The proportion of the Tibetan taurine genome inferred to be of yak ancestry is 1.2% per genome,and the estimated introgression time was ~1.9 kya.The enrichment analysis identified major enrichment of banteng introgressed genes involved in sensory perception and immunity,and yak introgressed genes involved sensory perception of smell and disease resistance.All those historic introgression events that impoved domestic cattle from Southern China and the Tibetan Plateau achieve rapid adaptation of tropical climate environments and hypoxic environment by acquiring genomic variations from Bos javanicus(banteng)and Bos grunniens(yak),respectively.All those showed that gene flow contributed to the environmental adaptation of cattle.4.Demographic history of East Asian cattle revealed that that two genetically differentiated wild B.indicus populations may have contributed to indicine ancestry or Chinese indicine cattle had input from a separate strain of Chinese or Southeast Asian aurochs through eastward migrationThe divergence time between B.taurus and B.indicus was estimated at approximately ~212 to 285 kya.The relative cross-coalescence analysis suggested a decline to 0.5 between East Asian taurine and Eurasian taurine or European taurine cattle at ~6.6 kya,suggesting that different expansion of agricultural societies brought domestic taurine cattle to other places,which formed the distinctive genomic characteristics.Two primary domestication centers in the Near East and The Indus Valley is considered as the primary domestication center of B.indicus cattle.However,we observed an earlier and clearly pre-domestication split ~ 49.6 kya between Chinese indicine and Indian indicine cattle,indicating that two genetically differentiated wild B.indicus populations may have contributed to indicine ancestry or Chinese indicine cattle had input from a separate strain of Chinese or Southeast Asian aurochs through eastward migration.