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.

Broad maternal geographic origin of domestic sheep in Anatolia and the Zagros.

We investigated the controversial origin of domestic sheep (Ovis aries) using large samples of contemporary and ancient domestic individuals and their closest wild relatives: the Asiatic mouflon (Ovis gmelini), the urial (Ovis vignei) and the argali (Ovis ammon). A phylogeny based on mitochondrial DNA, including 213 new cytochrome-b sequences of wild Ovism confirmed that O. gmelini is the maternal ancestor of sheep and precluded mtDNA contributions from O. vignei (and O. gmelini × O. vignei hybrids) to domestic lineages. We also produced 54 new control region sequences showing shared haplogroups (A, B, C and E) between domestic sheep and wild O. gmelini which localized the domestication center in eastern Anatolia and central Zagros, excluding regions further east where exclusively wild haplogroups were found. This overlaps with the geographic distribution of O. gmelini gmelini, further suggesting that the maternal origin of domestic sheep derives from this subspecies. Additionally, we produced 57 new CR sequences of Neolithic sheep remains from a large area covering Anatolia to Europe, showing the early presence of at least three mitochondrial haplogroups (A, B and D) in Western colonization routes. This confirmed that sheep domestication was a large-scale process that captured diverse maternal lineages (haplogroups).

Origins of house mice in ecological niches created by settled hunter-gatherers in the Levant 15,000 y ago.

Reductions in hunter-gatherer mobility during the Late Pleistocene influenced settlement ecologies, altered human relations with animal communities, and played a pivotal role in domestication. The influence of variability in human mobility on selection dynamics and ecological interactions in human settlements has not been extensively explored, however. This study of mice in modern African villages and changing mice molar shapes in a 200,000-y-long sequence from the Levant demonstrates competitive advantages for commensal mice in long-term settlements. Mice from African pastoral households provide a referential model for habitat partitioning among mice taxa in settlements of varying durations. The data reveal the earliest known commensal niche for house mice in long-term forager settlements 15,000 y ago. Competitive dynamics and the presence and abundance of mice continued to fluctuate with human mobility through the terminal Pleistocene. At the Natufian site of Ain Mallaha, house mice displaced less commensal wild mice during periods of heavy occupational pressure but were outcompeted when mobility increased. Changing food webs and ecological dynamics in long-term settlements allowed house mice to establish durable commensal populations that expanded with human societies. This study demonstrates the changing magnitude of cultural niche construction with varying human mobility and the extent of environmental influence before the advent of farming.

Regional asynchronicity in dairy production and processing in early farming communities of the northern Mediterranean.

In the absence of any direct evidence, the relative importance of meat and dairy productions to Neolithic prehistoric Mediterranean communities has been extensively debated. Here, we combine lipid residue analysis of ceramic vessels with osteo-archaeological age-at-death analysis from 82 northern Mediterranean and Near Eastern sites dating from the seventh to fifth millennia BC to address this question. The findings show variable intensities in dairy and nondairy activities in the Mediterranean region with the slaughter profiles of domesticated ruminants mirroring the results of the organic residue analyses. The finding of milk residues in very early Neolithic pottery (seventh millennium BC) from both the east and west of the region contrasts with much lower intensities in sites of northern Greece, where pig bones are present in higher frequencies compared with other locations. In this region, the slaughter profiles of all domesticated ruminants suggest meat production predominated. Overall, it appears that milk or the by-products of milk was an important foodstuff, which may have contributed significantly to the spread of these cultural groups by providing a nourishing and sustainable product for early farming communities.

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 evolution of dual meat and milk cattle husbandry in Linearbandkeramik societies.

Cattle dominate archaeozoological assemblages from the north-central Europe between the sixth and fifth millennium BC and are frequently considered as exclusively used for their meat. Dairy products may have played a greater role than previously believed. Selective pressure on the lactase persistence mutation has been modelled to have begun between 6000 and 4000 years ago in central Europe. The discovery of milk lipids in late sixth millennium ceramic sieves in Poland may reflect an isolated regional peculiarity for cheese making or may signify more generalized milk exploitation in north-central Europe during the Early Neolithic. To investigate these issues, we analysed the mortality profiles based on age-at-death analysis of cattle tooth eruption, wear and replacement from 19 archaeological sites of the Linearbandkeramik (LBK) culture (sixth to fifth millennium BC). The results indicate that cattle husbandry was similar across time and space in the LBK culture with a degree of specialization for meat exploitation in some areas. Statistical comparison with reference age-at-death profiles indicate that mixed husbandry (milk and meat) was practised, with mature animals being kept. The analysis provides a unique insight into LBK cattle husbandry and how it evolved in later cultures in central and western Europe. It also opens a new perspective on how and why the Neolithic way of life developed through continental Europe and how dairy products became a part of the human diet.

The genetic prehistory of domesticated cattle from their origin to the spread across Europe.

BACKGROUND: Cattle domestication started in the 9(th) millennium BC in Southwest Asia. Domesticated cattle were then introduced into Europe during the Neolithic transition. However, the scarcity of palaeogenetic data from the first European domesticated cattle still inhibits the accurate reconstruction of their early demography. In this study, mitochondrial DNA from 193 ancient and 597 modern domesticated cattle (Bos taurus) from sites across Europe, Western Anatolia and Iran were analysed to provide insight into the Neolithic dispersal process and the role of the local European aurochs population during cattle domestication. RESULTS: Using descriptive summary statistics and serial coalescent simulations paired with approximate Bayesian computation we find: (i) decreasing genetic diversity in a southeast to northwest direction, (ii) strong correlation of genetic and geographical distances, iii) an estimated effective size of the Near Eastern female founder population of 81, iv) that the expansion of cattle from the Near East and Anatolia into Europe does not appear to constitute a significant bottleneck, and that v) there is evidence for gene-flow between the Near Eastern/Anatolian and European cattle populations in the early phases of the European Neolithic, but that it is restricted after 5,000 BCE. CONCLUSIONS: The most plausible scenario to explain these results is a single and regionally restricted domestication process of cattle in the Near East with subsequent migration into Europe during the Neolithic transition without significant maternal interbreeding with the endogenous wild stock. Evidence for gene-flow between cattle populations from Southwestern Asia and Europe during the earlier phases of the European Neolithic points towards intercontinental trade connections between Neolithic farmers.

First wave of cultivators spread to Cyprus at least 10,600 y ago.

Early Neolithic sedentary villagers started cultivating wild cereals in the Near East 11,500 y ago [Pre-Pottery Neolithic A (PPNA)]. Recent discoveries indicated that Cyprus was frequented by Late PPNA people, but the earliest evidence until now for both the use of cereals and Neolithic villages on the island dates to 10,400 y ago. Here we present the recent archaeological excavation at Klimonas, which demonstrates that established villagers were living on Cyprus between 11,100 and 10,600 y ago. Villagers had stone artifacts and buildings (including a remarkable 10-m diameter communal building) that were similar to those found on Late PPNA sites on the mainland. Cereals were introduced from the Levant, and meat was obtained by hunting the only ungulate living on the island, a small indigenous Cypriot wild boar. Cats and small domestic dogs were brought from the mainland. This colonization suggests well-developed maritime capabilities by the PPNA period, but also that migration from the mainland may have occurred shortly after the beginning of agriculture.

Rethinking dog domestication by integrating genetics, archeology, and biogeography.

The dog was the first domesticated animal but it remains uncertain when the domestication process began and whether it occurred just once or multiple times across the Northern Hemisphere. To ascertain the value of modern genetic data to elucidate the origins of dog domestication, we analyzed 49,024 autosomal SNPs in 1,375 dogs (representing 35 breeds) and 19 wolves. After combining our data with previously published data, we contrasted the genetic signatures of 121 breeds with a worldwide archeological assessment of the earliest dog remains. Correlating the earliest archeological dogs with the geographic locations of 14 so-called "ancient" breeds (defined by their genetic differentiation) resulted in a counterintuitive pattern. First, none of the ancient breeds derive from regions where the oldest archeological remains have been found. Second, three of the ancient breeds (Basenjis, Dingoes, and New Guinea Singing Dogs) come from regions outside the natural range of Canis lupus (the dog's wild ancestor) and where dogs were introduced more than 10,000 y after domestication. These results demonstrate that the unifying characteristic among all genetically distinct so-called ancient breeds is a lack of recent admixture with other breeds likely facilitated by geographic and cultural isolation. Furthermore, these genetically distinct ancient breeds only appear so because of their relative isolation, suggesting that studies of modern breeds have yet to shed light on dog origins. We conclude by assessing the limitations of past studies and how next-generation sequencing of modern and ancient individuals may unravel the history of dog domestication.

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.

Pre-Neolithic wild boar management and introduction to Cyprus more than 11,400 years ago.

The beginnings of pig domestication in Southwest Asia are controversial. In some areas, it seems to have occurred abruptly ca. 10,500 years ago, whereas in nearby locations, it appears to have resulted from a long period of management of wild boar starting at the end of the Late Pleistocene. Here, we present analyses of suid bones from Akrotiri Aetokremnos, Cyprus. This site has provided the earliest evidence for human occupation of the Mediterranean islands. Morphological analysis and direct radiocarbon dating of both degraded collagen and apatite of these bones reveal that small-sized suids were living on Cyprus 11,400-11,700 years ago. We demonstrate that these suids were introduced by humans and that, at this early date, their small size must result from island isolation. This sheds light on the early Holocene colonization of Cyprus and on pre-Neolithic Mediterranean seafaring. We further argue that wild boar were managed on the mainland before their introduction to Cyprus (i.e., before the beginning of the Neolithic and at least 1 millennium before the earliest known morphological modifications attributable to domestication). This adds weight to the theory that pig domestication involved a long period of wild boar management that started about the time of the Pleistocene/Holocene transition.

Palaeogenomic analysis of black rat (Rattus rattus) reveals multiple European introductions associated with human economic history.

The distribution of the black rat (Rattus rattus) has been heavily influenced by its association with humans. The dispersal history of this non-native commensal rodent across Europe, however, remains poorly understood, and different introductions may have occurred during the Roman and medieval periods. Here, in order to reconstruct the population history of European black rats, we first generate a de novo genome assembly of the black rat. We then sequence 67 ancient and three modern black rat mitogenomes, and 36 ancient and three modern nuclear genomes from archaeological sites spanning the 1st-17th centuries CE in Europe and North Africa. Analyses of our newly reported sequences, together with published mitochondrial DNA sequences, confirm that black rats were introduced into the Mediterranean and Europe from Southwest Asia. Genomic analyses of the ancient rats reveal a population turnover in temperate Europe between the 6th and 10th centuries CE, coincident with an archaeologically attested decline in the black rat population. The near disappearance and re-emergence of black rats in Europe may have been the result of the breakdown of the Roman Empire, the First Plague Pandemic, and/or post-Roman climatic cooling.

The goat domestication process inferred from large-scale mitochondrial DNA analysis of wild and domestic individuals.

The emergence of farming during the Neolithic transition, including the domestication of livestock, was a critical point in the evolution of human kind. The goat (Capra hircus) was one of the first domesticated ungulates. In this study, we compared the genetic diversity of domestic goats to that of the modern representatives of their wild ancestor, the bezoar, by analyzing 473 samples collected over the whole distribution range of the latter species. This partly confirms and significantly clarifies the goat domestication scenario already proposed by archaeological evidence. All of the mitochondrial DNA haplogroups found in current domestic goats have also been found in the bezoar. The geographic distribution of these haplogroups in the wild ancestor allowed the localization of the main domestication centers. We found no haplotype that could have been domesticated in the eastern half of the Iranian Plateau, nor further to the east. A signature of population expansion in bezoars of the C haplogroup suggests an early domestication center on the Central Iranian Plateau (Yazd and Kerman Provinces) and in the Southern Zagros (Fars Province), possibly corresponding to the management of wild flocks. However, the contribution of this center to the current domestic goat population is rather low (1.4%). We also found a second domestication center covering a large area in Eastern Anatolia, and possibly in Northern and Central Zagros. This last domestication center is the likely origin of almost all domestic goats today. This finding is consistent with archaeological data identifying Eastern Anatolia as an important domestication center.

Bones geometric morphometrics illustrate 10th millennium cal. BP domestication of autochthonous Cypriot wild boar (Sus scrofa circeus nov. ssp).

Epipaleolithic hunter-gatherers from the Near East introduced wild boars (Sus scrofa) to Cyprus, with the Early Pre-Pottery Neolithic (PPN) settlers hunting the wild descendants of these boars. However, the geographic origin of the Cypriot boar and how they were integrated into the earliest forms of pig husbandry remain unsolved. Here, we present data on 11,000 to 9000 cal. BP Sus scrofa from the PPN sites of Klimonas and Shillourokambos. We compared them to contemporaneous populations from the Near East and to Neolithic and modern populations in Corsica, exploring their origin and evolution using biosystematic signals from molar teeth and heel bones (calcanei), using 2D and 3D geometric morphometrics. We found that the Cypriot PPN lineage of Sus scrofa originates from the Northern Levant. Yet, their phenotypic idiosyncrasy suggest that they evolved into an insular sub-species that we named Sus scrofa circeus, referring to Circe, the metamorphosis goddess that changed Ulysses companions into pigs. The phenotypic homogeneity among PPNA Klimonas wild boars and managed populations of PPNB Shillourokambos suggests that local domestication has been undertaken on the endemic S. s. circeus, strengthening the idea that Cyprus was integrated into the core region of animal domestication.

Early evidence of sheep lambing de-seasoning in the Western Mediterranean in the sixth millennium BCE.

Today, sheep farmers in the Western Mediterranean de-season their ewes to achieve autumnal births. This strategy contrasts sharply with spring lambing further north, and provides benefits in terms of out-of-season availability of animal products. These competences are closely linked to specific sheep physiology and favorable Western Mediterranean climatic conditions. It is not known exactly how far back in the past the ability to de-season Mediterranean sheep breeds extends. This study shows that this practice existed seven millennia ago in Southern France, at an early stage of the major agricultural expansion of the Neolithic into the Western Mediterranean. To achieve this reproductive management regime, three prerequisites were required: (i) the ability of sheep to give birth in autumn, constituting early evidence for the genetic selection of specimens with prolonged reproductive fertility; (ii) intentional management of female and male interactions within the herd, which would have required good knowledge of the timing of the fertility cycle in ewes, and; (iii) adequate pasture resources to support lactation in the autumn, possibly favored by autumnal rains, substantiating previous paleoclimatological data for the existence of a Mediterranean-type precipitation regime at that time. Moreover, we also show that winter foddering of sheep occurred, using forest resources, and that this maintained good body weights for spring mating. These findings add pivotal information about shepherding practices and the socio-economic abilities of Early Neolithic communities, which allowed for the extension of their areas of influence from the Eastern Mediterranean area to the West during the Early Neolithic agricultural expansion in Europe.

The mark of captivity: plastic responses in the ankle bone of a wild ungulate (Sus scrofa).

Deciphering the plastic (non-heritable) changes induced by human control over wild animals in the archaeological record is challenging. We hypothesized that changes in locomotor behaviour in a wild ungulate due to mobility control could be quantified in the bone anatomy. To test this, we experimented with the effect of mobility reduction on the skeleton of wild boar (Sus scrofa), using the calcaneus shape as a possible phenotypic marker. We first assessed differences in shape variation and covariation in captive-reared and wild-caught wild boars, taking into account differences in sex, body mass, available space for movement and muscle force. This plastic signal was then contrasted with the phenotypic changes induced by selective breeding in domestic pigs. We found that mobility reduction induces a plastic response beyond the shape variation of wild boars in their natural habitat, associated with a reduction in the range of locomotor behaviours and muscle loads. This plastic signal of captivity in the calcaneus shape differs from the main changes induced by selective breeding for larger muscle and earlier development that impacted the pigs' calcaneus shape in a much greater extent than the mobility reduction during the domestication process of their wild ancestors.

Tracking the Near Eastern origins and European dispersal of the western house mouse.

The house mouse (Mus musculus) represents the extreme of globalization of invasive mammals. However, the timing and basis of its origin and early phases of dispersal remain poorly documented. To track its synanthropisation and subsequent invasive spread during the develoment of complex human societies, we analyzed 829 Mus specimens from 43 archaeological contexts in Southwestern Asia and Southeastern Europe, between 40,000 and 3,000 cal. BP, combining geometric morphometrics numerical taxonomy, ancient mitochondrial DNA and direct radiocarbon dating. We found that large late hunter-gatherer sedentary settlements in the Levant, c. 14,500 cal. BP, promoted the commensal behaviour of the house mouse, which probably led the commensal pathway to cat domestication. House mouse invasive spread was then fostered through the emergence of agriculture throughout the Near East 12,000 years ago. Stowaway transport of house mice to Cyprus can be inferred as early as 10,800 years ago. However, the house mouse invasion of Europe did not happen until the development of proto urbanism and exchange networks - 6,500 years ago in Eastern Europe and 4000 years ago in Southern Europe - which in turn may have driven the first human mediated dispersal of cats in Europe.