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Presentation of the Murbodner cattle “Hugo family” with surviving aurochs P haplogroup mitochondria. (a) Photo of the bull named Hugo first identified with P haplotype mitogenome. (b) Reduced family tree of the members of the “Hugo family”, in which the positions of the individuals sequenced with haplotype P are marked as full yellow squares or circles, (c) Median‐joining network (mitogenome length of 16,344 bps) representing the relationship between P and few other haplogroups (R, Q and T3). Abbreviations: BRS, Bovine Reference Sequence (T3); DNK, Denmark; GBR, Great Britain; ITA, Italy; KOR, Korea; POL, Poland are associated with declared origin of sequences
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The contribution of domestic cattle in human societies is enormous, making cattle, along with other essential benefits, the economically most important domestic animal in the world today. To expand existing knowledge on cattle domestication and mitogenome diversity, we performed a comprehensive complete mitogenome analysis of the species (802 seque...
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Background
Reference genomes are essential in the analysis of genomic data. As the cost of sequencing decreases, multiple reference genomes are being produced within species to alleviate problems such as low mapping accuracy and reference allele bias in variant calling that can be associated with the alignment of divergent samples to a single refer...
Citations
... Theoretically, effective population size (N e ) for mDNA equals the number of females or a quarter of the nDNA N e , though these relationships depend on the sex ratio (Birky et al., 1983). In a recent study, (Cubric-Curik et al., 2022) inferred the demographic trend in N e for mDNA in cattle. They found that mDNA N e is increasing over time, which is opposite to results for nDNA in dairy cattle (Ma-cLeod et al., 2013), but in line with the large diversity observed in mDNA (~1,000 polymorphic sites out of 16,202 base pairs). ...
Mitochondria play a significant role in numerous cellular processes through proteins encoded by both the nuclear genome (nDNA) and mito genome (mDNA), and increasing evidence shows that traits of interest might be affected by mito-nuclear interactions. While the variation in nDNA is influenced by mutations and recombination of parental genomes, the variation in mDNA is solely driven by mutations. In addition, mDNA is inherited in a haploid form, from the dam. Cattle populations show significant variation in mDNA between and within breeds. Past research suggests that variation in mDNA accounts for 1–5% of the phenotypic variation in dairy traits. Here we simulated a dairy cattle breeding program to assess the impact of accounting for mDNA variation in pedigree-based and genome-based genetic evaluations on the accuracy of estimated breeding values for mDNA and nDNA components. We also examined the impact of alternative definitions of breeding values on genetic gain, including nDNA and mDNA components that both impact phenotype expression, but mDNA is inherited only maternally. We found that accounting for mDNA variation increased accuracy between +0.01 and +0.03 for different categories of animals, especially for young bulls (+0.03) and females without genotype data (between +0.01 and +0.03). Different scenarios of modeling and breeding value definition impacted genetic gain. The standard approach of ignoring mDNA variation achieved competitive genetic gain. Modeling, but not selecting on mDNA expectedly reduced genetic gain, while optimal use of mDNA variation recovered the genetic gain.
... Furthermore, goats, also believed to have had a unique domestication, exhibited a phylogeographic structure similar to the one in sheep before the post-Neolithic rise of the modern dominant haplogroup (49). In cattle, the two independently domesticated species (Bos taurus and Bos indicus) display a mitochondrial differentiation that is much higher than the observed among sheep populations, and their phylogeographic structure is heavily influenced by post-Neolithic introgression (50). Further criticisms of the multiple domestication hypothesis in sheep point out that the hypothesis equals haplogroups with populations while ignoring the diversity of the ancestral wild populations (48). . ...
Occupied between ~10,300 and 9300 years ago, the Pre-Pottery Neolithic site of Aşıklı Höyük in Central Anatolia went through early phases of sheep domestication. Analysis of 629 mitochondrial genomes from this and numerous sites in Anatolia, southwest Asia, Europe, and Africa produced a phylogenetic tree with excessive coalescences (nodes) around the Neolithic, a potential signature of a domestication bottleneck. This is consistent with archeological evidence of sheep management at Aşıklı Höyük which transitioned from residential stabling to open pasturing over a millennium of site occupation. However, unexpectedly, we detected high genetic diversity throughout Aşıklı Höyük’s occupation rather than a bottleneck. Instead, we detected a tenfold demographic bottleneck later in the Neolithic, which caused the fixation of mitochondrial haplogroup B in southwestern Anatolia. The mitochondrial genetic makeup that emerged was carried from the core region of early Neolithic sheep management into Europe and dominates the matrilineal diversity of both its ancient and the billion-strong modern sheep populations.
... Consistent with this, a recent study has found surviving aurochs mtDNA lineages in modern taurine cattle, namely in the alpine Murbodner breed in Austria. This again confirms that interbreeding happened and that it had a traceable impact on the local cattle population [43]. ...
... The inevitable degradation also prevents the transfer of new technologies of long-range sequencing to the ancient samples, although this progress greatly simplifies targeted resequencing in extant populations. This can be documented by a full mtDNA survey in a range of cattle breeds across Central Europe and related regions obtained by long-range sequencing [43]. ...
Although Europe was not a primary centre of cattle domestication, its expansion from the Middle East and subsequent development created a complex pattern of cattle breed diversity. Many isolated populations of local historical breeds still carry the message about the physical and genetic traits of ancient populations. Since the way of life of human communities starting from the eleventh millennium BP was strongly determined by livestock husbandry, the knowledge of cattle diversity through the ages is helpful in the interpretation of many archaeological findings. Historical cattle diversity is currently at the intersection of two leading directions of genetic research. Firstly, it is archaeogenetics attempting to recover and interpret the preserved genetic information directly from archaeological finds. The advanced archaeogenetic approaches meet with the population genomics of extant cattle populations. The immense amount of genetic information collected from living cattle, due to its key economic role, allows for reconstructing the genetic profiles of the ancient populations backwards. The present paper aims to place selected archaeogenetic, genetic, and genomic findings in the picture of cattle history in Central Europe, as suggested by archaeozoological and historical records. Perspectives of the methodical connection between the genetic approaches and the approaches of traditional archaeozoology, such as osteomorphology and osteometry, are discussed. The importance, actuality, and effectiveness of combining different approaches to each archaeological find, such as morphological characterization, interpretation of the historical context, and molecular data, are stressed.
... In general, taxa within the genus Bos can hybridize and produce fertile offspring (16) which may have facilitated and contributed to domestication, local adaptation and even speciation (5,(17)(18)(19). Mitochondrial DNA studies have previously indicated gene flow between domestic cattle and aurochs outside their domestication center (20)(21)(22)(23)(24) and more recently, genomic studies have shown the presence of European aurochs ancestry in modern taurine cattle breeds (25,26). Although cattle have represented a significant economic resource and a prominent cultural icon for millennia, and have been studied through aDNA for more than a decade (20,21,27), to date only a few aurochs' genomes have been sequenced (5,25). ...
... The specimen assigned to T1 (moo009a) is notable since this individual was previously used to argue for Bronze Age contact between Iberia and Africa, where the T1 haplogroup is thought to have originated (27,33). T4 is usually considered to be restricted to Asian breeds with rare finds in Europe, restricted to the Balkans (23). The presence of T4 in Chalcolithic Iberia suggests that this haplogroup must have been distributed across Western Europe at low frequencies in prehistory. ...
Cattle have been a valuable economic resource and cultural icon since prehistory. From the initial expansion of domestic cattle into Europe during the Neolithic period, taurine cattle (Bos taurus) and their wild ancestor, the aurochs (B. primigenius), had overlapping ranges leading to ample opportunities for intentional and unintentional hybridization. We performed a bioarchaeological analysis of 24 Bos remains from Iberia dating from the Mesolithic to the Roman period. The archaeogenomic dataset allows us to investigate the extent of domestic-wild hybridization over time, providing insight into the species’ behavior and human management by aligning changes with cultural and genomic transitions in the archaeological record. Our results show frequent hybridization during the Neolithic and Chalcolithic, likely reflecting a mix of hunting and herding or relatively unmanaged herds, with mostly male aurochs and female domestic cattle involved in hybridization. This is supported by isotopic evidence of ecological niche sharing, with only a few domestic cattle possibly being managed. The proportion of aurochs ancestry in domestic cattle remains relatively constant from about 4000 years ago, probably due to herd management and selection against hybrids, coinciding with other cultural transitions. The constant level of wild ancestry (~20%) continues into modern western European breeds including the Spanish Lidia breed which is bred for its aggressiveness and fighting ability, but does not display elevated levels of aurochs ancestry. This study takes a genomic glance at the impact of human actions and wild introgression in the establishment of cattle as one of the most important domestic species today.
... Both genetic and archaeological evidence suggest the possibility of additional domestication events, most notably in North Africa (6)(7)(8)(9), but the ability to conclusively recognize introgression over indigenous domestication remains largely unresolved. Regardless, wild introgression is acknowledged as critical to the development of modern lineages (10)(11)(12)(13)(14)(15). ...
... More broadly, our results show the persistence of aurochs ancestry through time, even in taurine cattle from the Xiongnu and Turkic periods, which suggests widespread intentional interbreeding. This goes beyond what we might expect from opportunistic mating with wild bulls during the early stages of introduction or periods of stress (12). The isotopic results support the possibility of indigenous aurochs management in Mongolia by ~7800 cal BP, with genetic evidence for interbreeding between aurochs and taurine herds by ~2900 cal BP. ...
... The earliest taurine cattle introduced to East Asia are known to have been used in dairying (43), which highlights the importance of female taurine lineages. Male based introgression in cattle has been previously posited for Eurasia and Africa (9,12,17), but the unreliability of Y-chromosome data and a lack of genome-wide studies for ancient samples has obfuscated the evidence. Previous work has underscored the importance of introgression in environmental adaptation during adoption of domesticates (5,12,15). ...
Unlabelled:
Societies in East Asia have utilized domesticated cattle for over 5000 years, but the genetic history of cattle in East Asia remains understudied. Genome-wide analyses of 23 ancient Mongolian cattle reveal that East Asian aurochs and ancient East Asian taurine cattle are closely related, but neither are closely related to any modern East Asian breeds. We observe binary variation in aurochs diet throughout the early Neolithic, and genomic evidence shows millennia of sustained male-dominated introgression. We identify a unique connection between ancient Mongolian aurochs and the European Hereford breed. These results point to the likelihood of human management of aurochs in Northeast Asia prior to and during the initial adoption of taurine cattle pastoralism.
One-sentence summary:
Ancient interbreeding of East Asian aurochs and cattle suggests management, but leaves no signature in modern eastern breeds.
... In general, taxa within the genus Bos can hybridize and produce fertile offspring (16) which may have facilitated and contributed to domestication, local adaptation and even speciation (5,(17)(18)(19). Mitochondrial DNA studies have previously indicated gene flow between domestic cattle and aurochs outside their domestication center (20)(21)(22)(23)(24) and more recently, genomic studies have shown the presence of European aurochs ancestry in modern taurine cattle breeds (25,26). Although cattle have represented a significant economic resource and a prominent cultural icon for millennia, and have been studied through aDNA for more than a decade (20,21,27), to date only a few aurochs' genomes have been sequenced (5,25). ...
... The specimen assigned to T1 (moo009a) is notable since this individual was previously used to argue for Bronze Age contact between Iberia and Africa, where the T1 haplogroup is thought to have originated (27,33). T4 is usually considered to be restricted to Asian breeds with rare finds in Europe, restricted to the Balkans (23). The presence of T4 in Chalcolithic Iberia suggests 3 . ...
Cattle have been a valuable economic resource and cultural icon since prehistory. From the initial expansion of domestic cattle into Europe during the Neolithic period, taurine cattle (Bos taurus) and their wild ancestor, the aurochs (B. primigenius), had overlapping ranges leading to ample opportunities for intentional and unintentional hybridization. We performed a bioarchaeological analysis of 24 Bos remains from Iberia dating from the Mesolithic to the Roman period. The archaeogenomic dataset allows us to investigate the extent of domestic-wild hybridization over time, providing insight into the species' behavior and human management by aligning changes with cultural and genomic transitions in the archaeological record. Our results show frequent hybridization during the Neolithic and Chalcolithic, likely reflecting a mix of hunting and herding or relatively unmanaged herds, with mostly male aurochs and female domestic cattle involved in hybridization. This is supported by isotopic evidence of ecological niche sharing, with only a few domestic cattle possibly being managed. The proportion of aurochs ancestry in domestic cattle remains relatively constant from about 4000 years ago, probably due to herd management and selection against hybrids, coinciding with other cultural transitions. The constant level of wild ancestry (~20%) continues into modern western European breeds including the Spanish Lidia breed which is bred for its aggressiveness and fighting ability, but does not display elevated levels of aurochs ancestry. This study takes a genomic glance at the impact of human actions and wild introgression in the establishment of cattle as one of the most important domestic species today.
... In addition to their functional and physiological effects on phenotypic variation, which is important for high productivity, mitochondrial DNA information can also be used for a variety of tasks, including genealogical verification with error detection in the pedigree (Oliehoek and Bijma 2009;Čačić et al., 2014), understanding domestication and phylogenetics (Bradley et al., 1996;Loftus et al., 1994;Verdugo et al., 2019), providing evidence for ancient introgression (Achili et al., 2008;Cubric-Curik et al., 2022;Schibler et al., 2014;Verdugo et al., 2019), estimating maternal demographics (Achili et al., 2008;Mannen et al., 2020;Olivieri et al., 2015), estimating maternal lineage diversity with analysis of population structure (Ginja et al., 2019;Di Lorenzo et al., 2018) and several other topics. ...
... Our original reference dataset was aligned to the bovine reference mitogenome sequence (GenBank accession number V00654, 16338bp) using the Clustal Omega program (Sievers et al., 2011), visualized using MEGA7 software (Kumar et al., 2016), and set to a length of 16388bp without indels. All mitogenomes in our reference dataset were classified respect to haplogroups using both MitoToolPy (Peng et al., 2015) and BEAST algorithms according to the procedures described in Cubric-Curik et al. (2022). ...
... At the same time, the classification algorithm implemented in Magellan v2.0 was able to correctly define haplogroups according to the classification of complete mitogenomes obtained in Cubric-Curik et al. (2022), as 100% empirical agreement (T 1 , T 2 , T 3 , T 5 , Q, P, and R haplotypes) was found for all samples that were additionally sequenced or that were in the same lineage as the verified sequenced samples. In classifying the "reduced haplotypes" from the non-training dataset from GenBank, we identified a wide range of haplogroups, including haplogroups T 4 and I, which were not present in our genotyped samples. ...
In contrast to nuclear markers routinely used for genomic selection, mitogenome information has been underutilized for breeding and biodiversity management of cattle populations. Our main goal was to promote the efficient use of mitogenome SNPs contained in commercial high-throughput SNP arrays. In collaboration with NEOGEN Genomics (Lincoln, NE, USA), we integrated 310 SNPs into the commercial GGP Bovine 100K SNP array. In doing so, we demonstrated how mitogenome SNPs can be used in high-throughput arrays to (i) analyze population structure and diversity, (ii) classify bovine haplogroups and identify introgression and/or upgrading, (iii) screen and identify pedigree defects, (iv) impute mitogenome information on maternal lineages to increase statistical power in estimating the effects of mitogenome variation on quantitative production traits, and (v) identify deleterious mutations found in humans. In addition, we have developed protocols and pipelines integrated with the Magellan v2.0 software to enable efficient and routine use of mitogenome information in cattle breeding and genetic diversity management. Finally, we have highlighted some other interesting opportunities for the use of mitogenome information in the near future.
... Based on default parameters, multiple sequence alignment was performed using the MAFFT program [36]. The best model and parameters refer to Cubric-Curik et al. [37]. The maximum likelihood tree was constructed using raxmlGUI (v.2.0.8) [38] with the bootstrap value set to 1000 and the chosen model was GTR + GAMMA. ...
... Previous studies suggest that haplogroup T2, which existed in Turkey and Serbia as early as approximately 8000-7000 yBP [53], may have been introduced to China from the northwest [3] and is now common in modern cattle in Iran, Iraq, Greece, and Italy [54]. As for haplogroup T4, it spread from the Eurasian steppe to China [3] and is commonly found in modern Chinese, Japanese and Korean cattle breeds [37,55]. Although the samples in this study from the Xiongnu burials are late in date, they at least demonstrate the presence of ancient T4 domestic cattle in the eastern Eurasian steppe, which may be associated with T4 cattle in northern China, and reveal that we need to collect much earlier samples from the Eurasian steppe region in the next step to observe the route of introduction of T4 domestic cattle and the spread of T2 domestic cattle. ...
Cattle are one of the six livestock species that have occupied an important place in Chinese history. Previous ancient DNA studies have indicated that Chinese taurine cattle (Bos taurus taurus) are exotic, but the exact route and diffusion by which they were introduced to China is unknown. In this study, we extracted the mitochondrial genomes of 34 cases of ancient taurine cattle (from the late Neolithic to Qin and Han dynasties) excavated from sites in northern China and the eastern Eurasian steppe, and successfully obtained 14 mitochondrial genome sequences. The results of ancient DNA analysis reveal that with cultural exchange and trade, there was close genetic exchange between domestic taurine cattle in different regions. The haplotypes shared by domestic cattle have genetic continuity, reflecting the strong cultural influence of the large capital city sites such as Taosi, Shimao and Erlitou on the surrounding areas. This study suggests that ancient northern Chinese taurine cattle may have accompanied the westward transmission of agricultural or painted pottery culture and thus had a maternal genetic contribution to modern Tibetan cattle.
... 16041-16271 and (Table S3). The identification of members of the T1 haplogroup based on short d-loop fragments is problematic [4] due to recurrent mutations or diagnostic motifs outside the d-loop. We defined T1 using SNPs at position 16050 together with position 16113. ...
... T3 variants are the most common haplotypes in this study and have been documented all over Europe based on both ancient and modern DNA [3,4,74]. Cattle carrying ...
... T3 variants are the most common haplotypes in this study and have been documented all over Europe based on both ancient and modern DNA [3,4,74]. Cattle carrying Q, cf. ...
Fluctuations in the size of taurine cattle (Bos taurus) have been regularly demonstrated using archaeozoological data from across time and space in Europe, and have been linked to cultural, social and economic changes, but little is known about whether phenotypic change is accompanied by changes in genetic diversity. Here, we performed PCR-typed analysis of the partial mtDNA d-loop fragments of 99 cattle from the Neolithic to Early Medieval times from a number of different sites across Switzerland, combining newly presented data with previously published data (n = 20). We found that most cattle included (84) were members of the common European macro-haplogroup T3. However, cattle belonging to the haplogroups T1, T2, Q and P were identified as early as the Neolithic period, before 2690 cal. BCE. The highest diversity was found in the Neolithic period, during the 1st century CE and during the 7th–8th centuries CE. Bottleneck phases with low genetic diversity were detected during the Late Iron Age and from the fifth to the seventh century CE. Based on the FST values, Horgen, Corded Ware and cattle populations from the seventh to the ninth century CE were plotted away from the clusters of all other populations. The periods with larger-sized cattle correspond with those of high mtDNA d-loop diversity. Phenotype and genotype both appear to respond to the same socio-economic and cultural processes.
... Molecular evidence of uniparental and autosomal markers has confirmed that taurine and indicine cattle are derived from two geographically separated and genetically differentiated aurochs progenitors from West and South Asia, respectively. Among modern cattle, there are seven major mitochondrial haplogroups (taurine T1, T2, T3, T4, and T5 as well as indicine I1 and I2) Lenstra et al. 2014;Xia et al. 2019a); the rare mitochondrial haplogroups E, R, P, Q and C, supporting sporadic aurochs introgressions Xia et al. 2021;Cubric-Curik et al. 2022); five Y chromosome haplogroups (taurine Y1, Y2a, and Y2b as well as indicine Y3a and Y3b) (Xia et al. 2019b;Cao et al. 2019;Edwards et al. 2011;Pérez-Pardal et al. 2018); and at least eight major autosomal ancestral groups (Chen et al. 2018a as follows: (1) African taurine cattle living in humid and sub-humid, tsetse fly-infested, tropical environments in West Africa (Gautier et al. 2009;Kim et al. 2017); (2) East Asian taurine cattle in Northeast Asia and the Qinghai-Tibetan Plateau, which are adapted to extremely cold and hypoxic environments, and some of them carry alleles arising from yak introgression (Chen et al. 2018a;Wu et al. 2018); (3) Eurasian taurine cattle in semiarid regions in Central Asia Kantanen et al. 2009); (4) European taurine cattle inhabiting temperate climates that carry alleles arising through admixture with European aurochs and are the ancestors of most globalized industrial breeds (Achilli et al. 2008;Daetwyler et al. 2014;Park et al. 2015); (5) Indian-Pakistani indicine cattle in hot and semiarid regions ); (6) African indicine cattle in semiarid East and Central Africa with a mixed ancestry of African taurine and South Asian indicine breeds (Bahbahani et al. 2017;Kim et al. 2017Kim et al. , 2020); (7) Diversified East Asian indicine cattle that inhabit hot-humid environments and carry alleles from other wild and/or domestic Asian bovine species (Chen et al. 2018a;Sinding et al. 2021); and (8) Indonesian breeds in hot-humid environments, which show a mix of indicine, banteng and/or Bali cattle ancestries (Mohamad et al. 2009;Sudrajad et al. 2020). For a more detailed and comprehensive classification of modern cattle, see Felius et al. (2011). ...
