Dairying, diseases and the evolution of lactase persistence in Europe.

In European and many African, Middle Eastern and southern Asian populations, lactase persistence (LP) is the most strongly selected monogenic trait to have evolved over the past 10,000 years1. Although the selection of LP and the consumption of prehistoric milk must be linked, considerable uncertainty remains concerning their spatiotemporal configuration and specific interactions2,3. Here we provide detailed distributions of milk exploitation across Europe over the past 9,000 years using around 7,000 pottery fat residues from more than 550 archaeological sites. European milk use was widespread from the Neolithic period onwards but varied spatially and temporally in intensity. Notably, LP selection varying with levels of prehistoric milk exploitation is no better at explaining LP allele frequency trajectories than uniform selection since the Neolithic period. In the UK Biobank4,5 cohort of 500,000 contemporary Europeans, LP genotype was only weakly associated with milk consumption and did not show consistent associations with improved fitness or health indicators. This suggests that other reasons for the beneficial effects of LP should be considered for its rapid frequency increase. We propose that lactase non-persistent individuals consumed milk when it became available but, under conditions of famine and/or increased pathogen exposure, this was disadvantageous, driving LP selection in prehistoric Europe. Comparison of model likelihoods indicates that population fluctuations, settlement density and wild animal exploitation-proxies for these drivers-provide better explanations of LP selection than the extent of milk exploitation. These findings offer new perspectives on prehistoric milk exploitation and LP evolution.

Unexpected morphological diversity in ancient dogs compared to modern relatives.

Dogs are among the most variable species today, but little is known about the morphological variability in the early phases of their history. The Neolithic transition to farming may have resulted in an early morphological diversification as a result of changes in the anthropic environment or intentional selection on specific morphologies. Here, we describe the variability and modularity in mandible form by comparing 525 dog mandibles from European archaeological sites ranging from 8100 to 3000 cal. BC to a reference sample of modern dogs, wolves, and dingoes. We use three-dimensional geometric morphometrics to quantify the form of complete and fragmented mandibles. We demonstrate that an important morphological variability already existed before the Bronze Age in Europe, yet the largest, smallest, most brachycephalic or dolichocephalic extant dogs have no equivalent in the archaeological sample, resulting in a lower variation compared to modern relatives. The covariation between the anterior and posterior parts of the mandible is lower in archaeological dogs, suggesting a low degree of intentional human selection in early periods. The mandible of modern and ancient dogs differs in functionally important areas, possibly reflecting differences in diet, competition, or the implication of ancient dogs in hunting or defence.

Dogs accompanied humans during the Neolithic expansion into Europe.

Near Eastern Neolithic farmers introduced several species of domestic plants and animals as they dispersed into Europe. Dogs were the only domestic species present in both Europe and the Near East prior to the Neolithic. Here, we assessed whether early Near Eastern dogs possessed a unique mitochondrial lineage that differentiated them from Mesolithic European populations. We then analysed mitochondrial DNA sequences from 99 ancient European and Near Eastern dogs spanning the Upper Palaeolithic to the Bronze Age to assess if incoming farmers brought Near Eastern dogs with them, or instead primarily adopted indigenous European dogs after they arrived. Our results show that European pre-Neolithic dogs all possessed the mitochondrial haplogroup C, and that the Neolithic and Post-Neolithic dogs associated with farmers from Southeastern Europe mainly possessed haplogroup D. Thus, the appearance of haplogroup D most probably resulted from the dissemination of dogs from the Near East into Europe. In Western and Northern Europe, the turnover is incomplete and haplogroup C persists well into the Chalcolithic at least. These results suggest that dogs were an integral component of the Neolithic farming package and a mitochondrial lineage associated with the Near East was introduced into Europe alongside pigs, cows, sheep and goats. It got diluted into the native dog population when reaching the Western and Northern margins of Europe.

The altitudinal mobility of wild sheep at the Epigravettian site of Kalavan 1 (Lesser Caucasus, Armenia): Evidence from a sequential isotopic analysis in tooth enamel.

Kalavan 1 is an Epigravettian hunting campsite in the Aregunyats mountain chain in northeastern Armenia (Lesser Caucasus). The site lies at an elevation of 1640 m in a bottleneck that controls the descent into the Barepat Valley from the alpine meadows above. The lithic and faunal assemblages show evidence of the production of hunting weapons, the hunting and targeting of wild sheep (Ovis orientalis), and the constitution of animal product reserves. A seasonal occupation of the site was proposed within a model of occupation by Epigravettian hunter-gatherers that involved a search for obsidian resources in high altitude sources from the spring to the summer and settling at Kalavan 1 at the end of summer or during autumn to coincide with the migration of wild herds from the alpine meadows to the valley. A key parameter of this model is wild sheep ethology, with a specifically seasonal vertical mobility, based on observations from contemporary mouflon populations from the surrounding areas. In this study, the vertical mobility of Paleolithic wild sheep was directly investigated through sequential isotope analysis (δ(18)O, δ(13)C) in teeth. A marked seasonality of birth is suggested that reflects a physiological adaptation to the strong environmental constraints of this mountainous region. Most importantly, a recurrent altitudinal mobility was demonstrated on a seasonal basis, which confirms that wild sheep migrated from lowland areas that they occupied in the winter and then moved to higher altitude meadows during the summer. Last, low inter-individual variability in the stable isotope sequences favors a hypothesis of accumulation for these faunal remains over a short time period. Overall, this new dataset strengthens the previous interpretations for Kalavan 1 and contributes to an understanding of the pattern of occupation of mountain territories by Epigravettian communities.

Impact of global environmental changes on the range contraction of Eurasian moose since the Late Pleistocene.

Climatic oscillations are considered primary factors influencing the distribution of various life forms on Earth. Large species adapted to cold climates are particularly vulnerable to extinction due to the climate changes. In our study, we investigated whether the temperature increase since the Late Pleistocene and the contraction of environmental niche during the Holocene were the main factors contributing to the decreasing range of moose (Alces alces) in Europe. We also examined whether there were significant differences in environmental conditions between areas inhabited by moose in Europe and Asia, that could support the division of moose into western and eastern forms, as suggested by genetic and morphological data. We analysed environmental conditions in locations of 655 subfossil and modern moose occurrences over the past 50,000 years in Eurasia. We found that the most limiting climatic factor for the moose distribution since the Late Pleistocene was July temperature. >90 % of moose records were found in areas where the mean summer temperature was below 19 °C, with July temperatures showing over 3 times narrower interquartile range compared to January temperatures. We identified significant differences in environmental conditions between areas inhabited by the European and Asiatic moose. In Europe, the species occurred in regions with milder climates, higher primary productivity, and more frequently within forest biomes compared to Asiatic individuals. The moose range shifted more in the west-east than in the south-north direction during the Holocene climate warming in Europe. We concluded that although the area of suitable moose habitat has increased since 12-8 ka years BP, as demonstrated by environmental niche modeling, the retreat of A. alces in large areas of Europe was likely caused by anthropogenic landscape change (e.g., deforestation) and overhunting by humans during the late Holocene rather than by climate warming during the Pleistocene to Holocene transition.

The Upper Palaeolithic site of Kalavan 1 (Armenia): an Epigravettian settlement in the Lesser Caucasus.

The open-air site of Kalavan 1 is located in the Aregunyats mountain chain (at 1640 m above sea level) on the northern bank of Lake Sevan. It is the first Upper Palaeolithic site excavated in Armenia. Led by an Armenian-French team, several excavations (2005-2009) have revealed a well preserved palaeosoil, dated to around 14,000 BP (years before present), containing fauna, lithic artefacts, as well as several hearths and activity areas that structure the settlement. The initial studies enable placement of the site in its environment and justify palaeoethnological analysis of the Epigravettian human groups of the Lesser Caucasus.

Seasonal calving in European Prehistoric cattle and its impacts on milk availability and cheese-making.

Present-day domestic cattle are reproductively active throughout the year, which is a major asset for dairy production. Large wild ungulates, in contrast, are seasonal breeders, as were the last historic representatives of the aurochs, the wild ancestors of cattle. Aseasonal reproduction in cattle is a consequence of domestication and herding, but exactly when this capacity developed in domestic cattle is still unknown and the extent to which early farming communities controlled the seasonality of reproduction is debated. Seasonal or aseasonal calving would have shaped the socio-economic practices of ancient farming societies differently, structuring the agropastoral calendar and determining milk availability where dairying is attested. In this study, we reconstruct the calving pattern through the analysis of stable oxygen isotope ratios of cattle tooth enamel from 18 sites across Europe, dating from the 6th mill. cal BC (Early Neolithic) in the Balkans to the 4th mill. cal BC (Middle Neolithic) in Western Europe. Seasonal calving prevailed in Europe between the 6th and 4th millennia cal BC. These results suggest that cattle agropastoral systems in Neolithic Europe were strongly constrained by environmental factors, in particular forage resources. The ensuing fluctuations in milk availability would account for cheese-making, transforming a seasonal milk supply into a storable product.

Taming the late Quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA.

Taxonomic over-splitting of extinct or endangered taxa, due to an incomplete knowledge of both skeletal morphological variability and the geographical ranges of past populations, continues to confuse the link between isolated extant populations and their ancestors. This is particularly problematic with the genus Equus. To more reliably determine the evolution and phylogeographic history of the endangered Asiatic wild ass, we studied the genetic diversity and inter-relationships of both extinct and extant populations over the last 100,000 years, including samples throughout its previous range from Western Europe to Southwest and East Asia. Using 229 bp of the mitochondrial hypervariable region, an approach which allowed the inclusion of information from extremely poorly preserved ancient samples, we classify all non-African wild asses into eleven clades that show a clear phylogeographic structure revealing their phylogenetic history. This study places the extinct European wild ass, E. hydruntinus, the phylogeny of which has been debated since the end of the 19th century, into its phylogenetic context within the Asiatic wild asses and reveals recent mitochondrial introgression between populations currently regarded as separate species. The phylogeographic organization of clades resulting from these efforts can be used not only to improve future taxonomic determination of a poorly characterized group of equids, but also to identify historic ranges, interbreeding events between various populations, and the impact of ancient climatic changes. In addition, appropriately placing extant relict populations into a broader phylogeographic and genetic context can better inform ongoing conservation strategies for this highly-endangered species.

Amy2B copy number variation reveals starch diet adaptations in ancient European dogs.

Extant dog and wolf DNA indicates that dog domestication was accompanied by the selection of a series of duplications on the Amy2B gene coding for pancreatic amylase. In this study, we used a palaeogenetic approach to investigate the timing and expansion of the Amy2B gene in the ancient dog populations of Western and Eastern Europe and Southwest Asia. Quantitative polymerase chain reaction was used to estimate the copy numbers of this gene for 13 ancient dog samples, dated to between 15 000 and 4000 years before present (cal. BP). This evidenced an increase of Amy2B copies in ancient dogs from as early as the 7th millennium cal. BP in Southeastern Europe. We found that the gene expansion was not fixed across all dogs within this early farming context, with ancient dogs bearing between 2 and 20 diploid copies of the gene. The results also suggested that selection for the increased Amy2B copy number started 7000 years cal. BP, at the latest. This expansion reflects a local adaptation that allowed dogs to thrive on a starch rich diet, especially within early farming societies, and suggests a biocultural coevolution of dog genes and human culture.

Genomic and archaeological evidence suggest a dual origin of domestic dogs.

The geographic and temporal origins of dogs remain controversial. We generated genetic sequences from 59 ancient dogs and a complete (28x) genome of a late Neolithic dog (dated to ~4800 calendar years before the present) from Ireland. Our analyses revealed a deep split separating modern East Asian and Western Eurasian dogs. Surprisingly, the date of this divergence (~14,000 to 6400 years ago) occurs commensurate with, or several millennia after, the first appearance of dogs in Europe and East Asia. Additional analyses of ancient and modern mitochondrial DNA revealed a sharp discontinuity in haplotype frequencies in Europe. Combined, these results suggest that dogs may have been domesticated independently in Eastern and Western Eurasia from distinct wolf populations. East Eurasian dogs were then possibly transported to Europe with people, where they partially replaced European Paleolithic dogs.

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.

Evidence of coat color variation sheds new light on ancient canids.

We have used a paleogenetics approach to investigate the genetic landscape of coat color variation in ancient Eurasian dog and wolf populations. We amplified DNA fragments of two genes controlling coat color, Mc1r (Melanocortin 1 Receptor) and CBD103 (canine-ß-defensin), in respectively 15 and 19 ancient canids (dogs and wolf morphotypes) from 14 different archeological sites, throughout Asia and Europe spanning from ca. 12 000 B.P. (end of Upper Palaeolithic) to ca. 4000 B.P. (Bronze Age). We provide evidence of a new variant (R301C) of the Melanocortin 1 receptor (Mc1r) and highlight the presence of the beta-defensin melanistic mutation (CDB103-K locus) on ancient DNA from dog-and wolf-morphotype specimens. We show that the dominant K(B) allele (CBD103), which causes melanism, and R301C (Mc1r), the variant that may cause light hair color, are present as early as the beginning of the Holocene, over 10,000 years ago. These results underline the genetic diversity of prehistoric dogs. This diversity may have partly stemmed not only from the wolf gene pool captured by domestication but also from mutations very likely linked to the relaxation of natural selection pressure occurring in-line with this process.