Early history of European domestic cattle as revealed by ancient DNA

We present an extensive ancient DNA analysis of mainly Neolithic cattle bones sampled from archaeological sites along the route of Neolithic expansion, from Turkey to North-Central Europe and Britain. We place this first reasonable population sample of Neolithic cattle mitochondrial DNA sequence diversity in context to illustrate the continuity of haplotype variation patterns from the first European domestic cattle to the present. Interestingly, the dominant Central European pattern, a starburst phylogeny around the modal sequence, T3, has a Neolithic origin, and the reduced diversity within this cluster in the ancient samples accords with their shorter history of post-domestic accumulation of mutation.     

The Origins of Domesticated Cattle

The origin of domestic cattle has perplexed archaeologists for more than a century. Researchers have proposed various theories, which offer alternative spatial and chronological models for the origin and spread of domesticated cattle. One point of discussion is whether domestic cattle had a single or multiple origins; however, most authorities considered that the first steps towards cattle domestication were taken in southwest Asia and that domesticated cattle entered Europe with pastoralists migrating from this region. Domesticated taurine cattle were thought to have entered Africa in successive waves from southwest Asia, while zebu cattle migrated into Africa at a later date from Arabia and the Indian subcontinent. Analysis of mitochondrial DNA (mtDNA) shows that taurine and zebu cattle divergence before the Holocene and were probably domesticated independently. Recent mtDNA sequence data shows that African and European taurine cattle were probably domesticated independently, but that there was a process of genetic introgression between taurine and zebu cattle in Africa. Ancient DNA studies over the last 10 years suggest that Northern European aurochsens apparently contributed little or nothing to domestic cattle while Southern European aurochsens apparently made a significant input. However, Middle Eastern aurochsen, unfortunately not typed yet, are expected to be to be very similar to European breeds as well, both because archeological data suggest that the major center of domestication for European Bos taurus breeds was the Fertile Crescent (9), and also because a mtDNA sequence from a Syrian specimen dated at 8,000–9,000 years ago shows a typical European haplotype found both in modern breeds and the Italian aurochsen. Evidence seems to suggest that small to moderate levels of local gene flow from wild Bos primigenius females in selected breeds were either accepted or may be reinforced by Neolithic breeders.     

Linkage disequilibrium in the North American Holstein population

Linkage disequilibrium was estimated using 7119 single nucleotide polymorphism markers across the genome and 200 animals from the North American Holstein cattle population. The analysis of maternally inherited haplotypes revealed strong linkage disequilibrium ( r ²   >   0.8) in genomic regions of ∼50 kb or less. While linkage disequilibrium decays as a function of genomic distance, genomic regions within genes showed greater linkage disequilibrium and greater variation in linkage disequilibrium compared with intergenic regions. Identification of haplotype blocks could characterize the most common haplotypes. Although maximum haplotype block size was over 1 Mb, mean block size was 26–113 kb by various definitions, which was larger than that observed in humans (∼10 kb). Effective population size of the dairy cattle population was estimated from linkage disequilibrium between single nucleotide polymorphism marker pairs in various haplotype ranges. Rapid reduction of effective population size of dairy cattle was inferred from linkage disequilibrium in recent generations. This result implies a loss of genetic diversity because of the high rate of inbreeding and high selection intensity in dairy cattle. The pattern observed in this study indicated linkage disequilibrium in the current dairy cattle population could be exploited to refine mapping resolution. Changes in effective population size during past generations imply a necessity of plans to maintain polymorphism in the Holstein population.     

Mitochondrial DNA analysis shows a Near Eastern Neolithic origin for domestic cattle and no indication of domestication of European aurochs

The extinct aurochs (Bos primigenius primigenius) was a large type of cattle that ranged over almost the whole Eurasian continent. The aurochs is the wild progenitor of modern cattle, but it is unclear whether European aurochs contributed to this process. To provide new insights into the demographic history of aurochs and domestic cattle, we have generated high-confidence mitochondrial DNA sequences from 59 archaeological skeletal finds, which were attributed to wild European cattle populations based on their chronological date and/or morphology. All pre-Neolithic aurochs belonged to the previously designated P haplogroup, indicating that this represents the Late Glacial Central European signature. We also report one new and highly divergent haplotype in a Neolithic aurochs sample from Germany, which points to greater variability during the Pleistocene. Furthermore, the Neolithic and Bronze Age samples that were classified with confidence as European aurochs using morphological criteria all carry P haplotype mitochondrial DNA, suggesting continuity of Late Glacial and Early Holocene aurochs populations in Europe. Bayesian analysis indicates that recent population growth gives a significantly better fit to our data than a constant-sized population, an observation consistent with a postglacial expansion scenario, possibly from a single European refugial population. Previous work has shown that most ancient and modern European domestic cattle carry haplotypes previously designated T. This, in combination with our new finding of a T haplotype in a very Early Neolithic site in Syria, lends persuasive support to a scenario whereby gracile Near Eastern domestic populations, carrying predominantly T haplotypes, replaced P haplotype-carrying robust autochthonous aurochs populations in Europe, from the Early Neolithic onward. During the period of coexistence, it appears that domestic cattle were kept separate from wild aurochs and introgression was extremely rare.     

Y-SNPs do not indicate hybridisation between European aurochs and domestic cattle

Background

Previous genetic studies of modern and ancient mitochondrial DNA have confirmed the Near Eastern origin of early European domestic cattle. However, these studies were not able to test whether hybridisation with male aurochs occurred post-domestication. To address this issue, Götherström and colleagues (2005) investigated the frequencies of two Y-chromosomal haplotypes in extant bulls. They found a significant influence of wild aurochs males on domestic populations thus challenging the common view on early domestication and Neolithic stock-rearing. To test their hypothesis, we applied these Y-markers on Neolithic bone specimens from various European archaeological sites.

Methods and Findings

Here, we have analysed the ancient DNA of 59 Neolithic skeletal samples. After initial molecular sexing, two segregating Y-SNPs were identified in 13 bulls. Strikingly, our results do not support the hypothesis that these markers distinguish European aurochs from domesticated cattle.

Conclusions

The model of a rapid introduction of domestic cattle into Central Europe without significant crossbreeding with local wild cattle remains unchallenged.     

Modern taurine cattle descended from small number of near-eastern founders

Archaeozoological and genetic data indicate that taurine cattle were first domesticated from local wild ox (aurochs) in the Near East some 10,500 years ago. However, while modern mitochondrial DNA (mtDNA) variation indicates early Holocene founding event(s), a lack of ancient DNA data from the region of origin, variation in mutation rate estimates, and limited application of appropriate inference methodologies have resulted in uncertainty on the number of animals first domesticated. A large number would be expected if cattle domestication was a technologically straightforward and unexacting region-wide phenomenon, while a smaller number would be consistent with a more complex and challenging process. We report mtDNA sequences from 15 Neolithic to Iron Age Iranian domestic cattle and, in conjunction with modern data, use serial coalescent simulation and approximate Bayesian computation to estimate that around 80 female aurochs were initially domesticated. Such a low number is consistent with archaeological data indicating that initial domestication took place in a restricted area and suggests the process was constrained by the difficulty of sustained managing and breeding of the wild progenitors of domestic cattle.     

Health status of the Neolithic population of Alepotrypa Cave, Greece

During the Neolithic, human health and lifestyle changed following the adoption of domesticated plants and animals and sedentism. This paper presents a study on human osteological remains from Alepotrypa Cave, an important and very well-preserved Late and Final Greek Neolithic site occupied from 5000-3200 BC. The Alepotrypa sample comes from primary and secondary burials as well as scattered bone, and consists of a minimum number of 161 individuals. It includes equal proportions of adults and subadults and males and females, is characterized by high child mortality, and falls within the range of other Neolithic sites in terms of age profiles and stature. The most frequent pathological conditions observed in this population are: 1) anemic conditions (cribra orbitalia and porotic hyperostosis), mild or healed in manifestation, most probably of nutritional origin, resulting from a poor diet focused on terrestrial resources such as domesticated cereals; 2) osteoarthritis and musculoskeletal stress markers, indicative of increased physical activity and heavy workloads; and 3) elevated prevalence of healed, depressed cranial fractures, serving as evidence of violent, nonlethal confrontations. Teeth exhibit a low prevalence of dental carries and linear enamel hypoplasia. The overall demographic, pathological, and behavioral results are consistent with observations of Neolithic populations elsewhere in Greece and the Mediterranean.     

群体遗传学下动物驯化研究进展

动物驯化是将野生动物改变为能够长期稳定饲养的家养动物的过程。作为新石器时代农业革命的内容,驯化是人类社会文明进步的重要标志之一。由于和人类的密切关系,驯化不仅改变了动物的野生状态,也改变了人类的生活习性和文明进程。动物驯化研究的关键问题包含驯化祖先是谁、驯化所产生的改变及驯化时间地点等。随着高通量基因组技术和对应分析方法的发展,目前研究动物驯化一般基于群体水平,在群体遗传学的框架下研究动物驯化过程中的重要事件。本文总结了群体遗传学下动物驯化研究的相关内容,包括群体动态历史、选择信号、基因交流等,着重介绍了基因选择初始时间和基因交流时间两个新的拓展内容及分析方法,概述了家猪(Sus scrofa f. domestica)、家鸡(Gallus gallus domesticus)、绵羊(Ovis aries)和山羊(Caprine hircus)等几种主要农业动物近期驯化研究的进展,以期为动物驯化研究提供了新的方向和视角。     

Genomics at the origins of agriculture,part one

The causes and consequences of the Neolithic revolution represent a fundamental problem for anthropological inquiry. Traditional archeological evidence, ethnobotanical remains, artifacts, and settlement patterns have been used to infer the transition from foraging to primary food production. Recent advances in genomics (the study of the sequence, structure, and function of the genome) has enhanced our understanding of the process of plant and animal domestication, revealed the impact that adaptation to agriculture has had on human biology, and provided clues to the pathogens and parasites thought to have emerged during the Neolithic. Genomic analysis provides insights into the complexity of the process of domestication that may not be apparent from the physical remains of bones and seeds, and allows us to measure the impact that the shift to primary food production had on the human genome. Questions related to the location and the process of domestication can be answered more fully by analyzing the genomes of the plants and animals brought under human control. The spread of the agriculture package (plants, animals, and technology) by cultural diffusion or demic expansion can also be investigated through this approach. Whether dissemination by farmers or the diffusion of farming knowledge and technology was the source of the Neolithic expansion, this process should be revealed by the patterh of genetic and linguistic diversity and language found from centers of agricultural Neolithic development. In addition, a number of pathogens that were previously thought to have been transmitted from domesticated species to human now appear to have been present in foragers long before the agricultural revolution took place. Furthermore, we now have evidence that humans were the source of the transmission of some parasites to domesticated animals. For all of these reasons, data from genomic studies are providing a more complete understanding of the origins of agriculture, a critical hallmark in human evolution.     

The Prey Pathway: A Regional History of Cattle (Bos taurus) and Pig (Sus scrofa) Domestication in the Northern Jordan Valley,Israel

The faunal assemblage from the 9^th-8^th millennium BP site at Sha''ar Hagolan, Israel, is used to study human interaction with wild suids and cattle in a time period just before the appearance of domesticated animals of these species in the Jordan Valley. Our results, based on demographic and osteometric data, indicate that full domestication of both cattle and suids occurred at the site during the 8^th millennium. Importantly, domestication was preceded in both taxa by demographic and metric population parameters indicating severe overhunting. The possible role of overhunting in shaping the characteristics of domesticated animals and the social infrastructure to ownership of herds is then explored.     

A dig into the past mitochondrial diversity of Corsican goats reveals the influence of secular herding practices

The goat (Capra hircus) is one of the earliest domesticated species ca. 10,500 years ago in the Middle-East where its wild ancestor, the bezoar (Capra aegagrus), still occurs. During the Neolithic dispersal, the domestic goat was then introduced in Europe, including the main Mediterranean islands. Islands are interesting models as they maintain traces of ancient colonization, historical exchanges or of peculiar systems of husbandry. Here, we compare the mitochondrial genetic diversity of both medieval and extant goats in the Island of Corsica that presents an original and ancient model of breeding with free-ranging animals. We amplified a fragment of the Control Region for 21 medieval and 28 current goats. Most of them belonged to the A haplogroup, the most worldwide spread and frequent today, but the C haplogroup is also detected at low frequency in the current population. Present Corsican goats appeared more similar to medieval goats than to other European goat populations. Moreover, 16 out of the 26 haplotypes observed were endemic to Corsica and the inferred demographic history suggests that the population has remained constant since the Middle Ages. Implications of these results on management and conservation of endangered Corsican goats currently decimated by a disease are addressed.     

Phylogeography of the last surviving populations of Rhodian and Anatolian fallow deer (Dama dama dama L., 1758)

The European fallow deer ( Dama dama dama ) is one of the most widespread cervids, and its distribution has been heavily affected by man. At present, only one wild autochthonous population is reputed to survive in Anatolia, but its census size is dramatically decreasing. This means that a significant portion of the ancestral genetic diversity of this taxon is seriously threatened. In the present study, a portion of the mitochondrial DNA (D-loop) in 37 D. d. dama specimens from three Mediterranean sites, Turkey, the island of Rhodes (Greece), and the Italian Peninsula, and seven individuals of the Persian fallow deer, Dama dama mesopotamica , was sequenced, and the results from the data analysis are interpreted in light of current archaeozoological and biogeographical knowledge. We conclude that: (1) D. d. mesopotamica is strongly differentiated from D. d. dama , confirming the results of previous genetic studies and (2) the Rhodian populations of D. d. dama , founded by humans in Neolithic times, possess a set of mitochondrial lineages, found in no other study populations. The persistence of these haplotypes is particularly significant because human-mediated processes (e.g. domestication) usually result in genetic depletion and erosion of an ancestral genetic pool. In the case of the Rhodes' population of fallow deer, we hypothesize that, during the foundation of this population, humans unknowingly preserved a remarkable portion of the original genetic diversity of the source population(s).  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 835–844.     

Histomorphometric study of bone microstructure of primates and domestic animal with the goal of species identification with reference to the effects of domestication

Functional bone microstructure of long limb bones is a function of species-specific biomechanical properties such as locomotion and weight. Histomorphometry and statistics were used to identify various primate species (Hylobates moloch, Pongo satyrus borneensis, Pan tr. troglodytes, Gorilla g. gorilla, Homo sapiens), equid species (Equus caballus, Equus asinus, Equus mulus, Equus hemionus kulan, Equus ferus przewalskii) and also extinct horses e.g. iron age, medieval and neolithic forms on the microstructural level. Furthermore, bones from domesticated cattle, their Neolithic forms, pigs, sheep and goats (Bos taurus, Sus scrofa, Ovis aries, Capra hircus) were examined. Thin sections from proximal metacarpi or radii per species were taken in case of the domesticated animals and from distal humeri in case of the primates. Areas, perimeters, minimal and maximal axis of Haversian canals and secondary osteons were measured on digital images. Canonical discriminant analysis permits a differentiation of the species by these parameters of bone microstructure. Thus it is possible to distinguish between the different primate species, sheep and goats, horses, extinct horses, donkeys, mules and kulans on the microstructural level, however not between cattle and pig, E. f. przewalskii and Equus caballus, medieval and iron age horses. Neolithic cattle and horses do overlap, yet they are different from the modern forms.     

Many neglected tropical diseases may have originated in the Paleolithic or before: new insights from genetics

The standard view of modern human infectious diseases is that many of them arose during the Neolithic when animals were first domesticated, or afterwards. Here we review recent genetic and molecular clock estimates that point to a much older Paleolithic origin (2.5 million years ago to 10,000 years ago) of some of these diseases. During part of this ancient period our early human ancestors were still isolated in Africa. We also discuss the need for investigations of the origin of these diseases in African primates and other animals that have been the original source of many neglected tropical diseases.     

Differentiation of European cattle by AFLP fingerprinting

The Neolithic introduction of domestic cattle into Europe was followed by differential adaptation, selection, migration and genetic isolation, leading ultimately to the emergence of specialized breeds. We have studied the differentiation of European cattle by amplified fragment length polymorphism (AFLP) fingerprinting. Combining AFLP data sets from two laboratories yielded 81 biallelic polymorphic markers scored in 19-22 individual animals from 51 breeds. Model-based clustering differentiated Podolian cattle as well as French and Alpine breeds from other European cattle. AFLP genetic distances correlated well with microsatellite-based genetic distances calculated for the same breeds. However, the AFLP data emphasized the divergence of taurine and indicine cattle relative to the variation among European breeds and indicated an Eastern influence on Italian and Hungarian Podolian breeds. This probably reflects import from the East after the original introduction of domestic cattle into Europe. Our data suggest that Italian cattle breeds are relatively diverse at the DNA sequence level.     

Ciliated protozoa in the rumen of Turkish domestic cattle (Bos taurus L.)

ABSTRACT. Rumen Contents obtained from 28 domesticated cattle ( Bos taurus L.) slaughtered at abatoirs near Izmir, Turkey were surveyed for ciliate protozoa. Protozoa are known to make an appreciable contribution to ruminal fiber digestion in many different geographical areas; however, little if any Information is available on their occurrence in Turkish cattle. As a result of our survey, 13 genera including 52 species were identified. Nine of the species were further divided into 36 forma. The average ciliate density in our cattle (52.44 X 10⁴/ml) was higher than that of Turkish domestic sheep and other domestic cattle reported previously from different geographical areas. Entodinium basoglui, Entodinium williamsi f. williamsi, E. williamsi f. turcicum, E. dalli f. rudidorsospinatum, Entodinium imai, Entodinium oektemae, Eudiplodinium dehorityi, Epidinium graini, Ophryoscolex purkynjei f. bifidobicinctus , and Ophryoscolex purkynjei f. bifidoquadricinctus have previously been reported from Turkey and appear to be endemic. All of the remaining species represent a new host record for domestic Turkish cattle. This study also reports for the second time the presence of Entodinium constrictum in herbivorous mammals, and is the first record of its occurrence in domesticated cattle.     

Worldwide Patterns of Ancestry,Divergence, and Admixture in Domesticated Cattle

The domestication and development of cattle has considerably impacted human societies, but the histories of cattle breeds and populations have been poorly understood especially for African, Asian, and American breeds. Using genotypes from 43,043 autosomal single nucleotide polymorphism markers scored in 1,543 animals, we evaluate the population structure of 134 domesticated bovid breeds. Regardless of the analytical method or sample subset, the three major groups of Asian indicine, Eurasian taurine, and African taurine were consistently observed. Patterns of geographic dispersal resulting from co-migration with humans and exportation are recognizable in phylogenetic networks. All analytical methods reveal patterns of hybridization which occurred after divergence. Using 19 breeds, we map the cline of indicine introgression into Africa. We infer that African taurine possess a large portion of wild African auroch ancestry, causing their divergence from Eurasian taurine. We detect exportation patterns in Asia and identify a cline of Eurasian taurine/indicine hybridization in Asia. We also identify the influence of species other than Bos taurus taurus and B. t. indicus in the formation of Asian breeds. We detect the pronounced influence of Shorthorn cattle in the formation of European breeds. Iberian and Italian cattle possess introgression from African taurine. American Criollo cattle originate from Iberia, and not directly from Africa with African ancestry inherited via Iberian ancestors. Indicine introgression into American cattle occurred in the Americas, and not Europe. We argue that cattle migration, movement and trading followed by admixture have been important forces in shaping modern bovine genomic variation.     

Unravelling the complexity of domestication: a case study using morphometrics and ancient DNA analyses of archaeological pigs from Romania

Current evidence suggests that pigs were first domesticated in Eastern Anatolia during the ninth millennium cal BC before dispersing into Europe with Early Neolithic farmers from the beginning of the seventh millennium. Recent ancient DNA (aDNA) research also indicates the incorporation of European wild boar into domestic stock during the Neolithization process. In order to establish the timing of the arrival of domestic pigs into Europe, and to test hypotheses regarding the role European wild boar played in the domestication process, we combined a geometric morphometric analysis (allowing us to combine tooth size and shape) of 449 Romanian ancient teeth with aDNA analysis. Our results firstly substantiate claims that the first domestic pigs in Romania possessed the same mtDNA signatures found in Neolithic pigs in west and central Anatolia. Second, we identified a significant proportion of individuals with large molars whose tooth shape matched that of archaeological (likely) domestic pigs. These large ‘domestic shape’ specimens were present from the outset of the Romanian Neolithic (6100–5500 cal BC) through to later prehistory, suggesting a long history of admixture between introduced domestic pigs and local wild boar. Finally, we confirmed a turnover in mitochondrial lineages found in domestic pigs, possibly coincident with human migration into Anatolia and the Levant that occurred in later prehistory.     

Complete mitochondrial genomes reveal neolithic expansion into Europe

The Neolithic transition from hunting and gathering to farming and cattle breeding marks one of the most drastic cultural changes in European prehistory. Short stretches of ancient mitochondrial DNA (mtDNA) from skeletons of pre-Neolithic hunter-gatherers as well as early Neolithic farmers support the demic diffusion model where a migration of early farmers from the Near East and a replacement of pre-Neolithic hunter-gatherers are largely responsible for cultural innovation and changes in subsistence strategies during the Neolithic revolution in Europe. In order to test if a signal of population expansion is still present in modern European mitochondrial DNA, we analyzed a comprehensive dataset of 1,151 complete mtDNAs from present-day Europeans. Relying upon ancient DNA data from previous investigations, we identified mtDNA haplogroups that are typical for early farmers and hunter-gatherers, namely H and U respectively. Bayesian skyline coalescence estimates were then used on subsets of complete mtDNAs from modern populations to look for signals of past population expansions. Our analyses revealed a population expansion between 15,000 and 10,000 years before present (YBP) in mtDNAs typical for hunters and gatherers, with a decline between 10,000 and 5,000 YBP. These corresponded to an analogous population increase approximately 9,000 YBP for mtDNAs typical of early farmers. The observed changes over time suggest that the spread of agriculture in Europe involved the expansion of farming populations into Europe followed by the eventual assimilation of resident hunter-gatherers. Our data show that contemporary mtDNA datasets can be used to study ancient population history if only limited ancient genetic data is available.     

Characterisation of the substrate specificity of homogeneous vaccinia virus uracil-DNA glycosylase

The decision to stop smallpox vaccination and the loss of specific immunity in a large proportion of the population could jeopardise world health due to the possibility of a natural or provoked re-emergence of smallpox. Therefore, it is mandatory to improve the current capability to prevent or treat such infections. The DNA repair protein uracil-DNA glycosylase (UNG) is one of the viral enzymes important for poxvirus pathogenesis. Consequently, the inhibition of UNG could be a rational strategy for the treatment of infections with poxviruses. In order to develop inhibitor assays for UNG, as a first step, we have characterised the recombinant vaccinia virus UNG (vUNG) and compared it with the human nuclear form (hUNG2) and catalytic fragment (hUNG) UNG. In contrast to hUNG2, vUNG is strongly inhibited in the presence of 7.5 mM MgCl₂. We have shown that highly purified vUNG is not inhibited by a specific uracil-DNA glycosylase inhibitor. Interestingly, both viral and human enzymes preferentially excise uracil when it is opposite to cytosine. The present study provides the basis for the design of specific inhibitors for vUNG.