Ophélie Lebrasseur

Genomic and archaeological evidence suggest a dual origin of domestic dogs

A dogged investigation of domestication The history of how wolves became our pampered pooches of today has remained controversial. Frantz et al. describe high-coverage sequencing of the genome of an Irish dog from the Bronze Age as well as ancient dog mitochondrial DNA sequences. Comparing ancient dogs to a modern worldwide panel of dogs shows an old, deep split between East Asian and Western Eurasian dogs. Thus, dogs were domesticated from two separate wolf populations on either side of the Old World. Science, this issue p. 1228 Dogs may have been domesticated independently in Eastern and Western Eurasia from distinct wolf populations. 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.

Using ancient DNA to study the origins and dispersal of ancestral Polynesian chickens across the Pacific

Significance Ancient DNA sequences from chickens provide an opportunity to study their human-mediated dispersal across the Pacific due to the significant genetic diversity and range of archaeological material available. We analyze ancient and modern material and reveal that previous studies have been impacted by contamination with modern chicken DNA and, that as a result, there is no evidence for Polynesian dispersal of chickens to pre-Columbian South America. We identify genetic markers of authentic ancient Polynesian chickens and use them to model early chicken dispersals across the Pacific. We find connections between chickens in the Micronesian and Bismarck Islands, but no evidence these were involved in dispersals further east. We also find clues about the origins of Polynesian chickens in the Philippines. The human colonization of Remote Oceania remains one of the great feats of exploration in history, proceeding east from Asia across the vast expanse of the Pacific Ocean. Human commensal and domesticated species were widely transported as part of this diaspora, possibly as far as South America. We sequenced mitochondrial control region DNA from 122 modern and 22 ancient chicken specimens from Polynesia and Island Southeast Asia and used these together with Bayesian modeling methods to examine the human dispersal of chickens across this area. We show that specific techniques are essential to remove contaminating modern DNA from experiments, which appear to have impacted previous studies of Pacific chickens. In contrast to previous reports, we find that all ancient specimens and a high proportion of the modern chickens possess a group of unique, closely related haplotypes found only in the Pacific. This group of haplotypes appears to represent the authentic founding mitochondrial DNA chicken lineages transported across the Pacific, and allows the early dispersal of chickens across Micronesia and Polynesia to be modeled. Importantly, chickens carrying this genetic signature persist on several Pacific islands at high frequencies, suggesting that the original Polynesian chicken lineages may still survive. No early South American chicken samples have been detected with the diagnostic Polynesian mtDNA haplotypes, arguing against reports that chickens provide evidence of Polynesian contact with pre-European South America. Two modern specimens from the Philippines carry haplotypes similar to the ancient Pacific samples, providing clues about a potential homeland for the Polynesian chicken.

Questioning new answers regarding Holocene chicken domestication in China

Xiang et al. (1) assert that chickens were domesticated on the North China plain 10,000 y ago. Although a great deal remains unknown about the temporal and geographic origins of poultry husbandry, this claim is extraordinary. We welcome the increasing application of modern bioarcheological techniques to questions pertaining to animal domestication in China, but we are skeptical about these conclusions for several reasons.

Inferring allele frequency trajectories from ancient DNA indicates that selection on a chicken gene coincided with changes in medieval husbandry practices

Abstract Ancient DNA provides an opportunity to infer the drivers of natural selection by linking allele frequency changes to temporal shifts in environment or cultural practices. However, analyses have often been hampered by uneven sampling and uncertainties in sample dating, as well as being confounded by demographic processes. Here, we present a Bayesian statistical framework for quantifying the timing and strength of selection using ancient DNA that explicitly addresses these challenges. We applied this method to time series data for two loci: TSHR and BCDO2, both hypothesised to have undergone strong and recent selection in domestic chickens. The derived variant in TSHR, associated with reduced aggression to conspecifics and faster onset of egg laying, shows strong selection beginning around 1,100 years ago, coincident with archaeological evidence for intensified chicken production and documented changes in egg and chicken consumption. To our knowledge, this is the first example of preindustrial domesticate trait selection in response to a historically attested cultural shift in food preference. For BCDO2, we find support for selection, but demonstrate that the recent rise in allele frequency could also have been driven by gene flow from imported Asian chickens during more recent breed formations. Our findings highlight that traits found ubiquitously in modern domestic species may not necessarily have originated during the early stages of domestication. In addition, our results demonstrate the importance of precise estimation of allele frequency trajectories through time for understanding the drivers of selection.

Reply to Beavan, Bryant, and Storey and Matisoo-Smith: Ancestral Polynesian “D” haplotypes reflect authentic Pacific chicken lineages

None of the letters in response to Thomson et al. (1) undermine our conclusions. However, several issues have been raised, which we address in this reply. Beavan (2) dismisses some of the concerns that have been raised about the accuracy of the radiocarbon dates of the El Arenal-1 chicken bones, which are immediately pre-Columbian. Although procedures, such as ultrafiltration of amino acids, are common practice for suboptimal bone samples, such as the oldest El Arenal-1 sample, further complex issues, including dietary sources and the potential for indirect marine carbon input (3), mean that a detailed assessment of the site through multiple further dates would be required to exclude the possibility that the specimens might actually be post-Columbian. This approach seems particularly advisable given that analogous issues were raised about a surprisingly early date for New Zealand colonization based on Pacific rat bone dates generated at the same laboratory using similar procedures (4), which were subsequently shown to be erroneously old (5).

The evolutionary history of dogs in the Americas

Lineage losses for mans best friend Dogs have been present in North America for at least 9000 years. To better understand how present-day breeds and populations reflect their introduction to the New World, Ní Leathlobhair et al. sequenced the mitochondrial and nuclear genomes of ancient dogs (see the Perspective by Goodman and Karlsson). The earliest New World dogs were not domesticated from North American wolves but likely originated from a Siberian ancestor. Furthermore, these lineages date back to a common ancestor that coincides with the first human migrations across Beringia. This lineage appears to have been mostly replaced by dogs introduced by Europeans, with the primary extant lineage remaining as a canine transmissible venereal tumor. Science, this issue p. 81; see also p. 27 Ancient North American dogs survive primarily as a canine transmissible venereal tumor. Dogs were present in the Americas before the arrival of European colonists, but the origin and fate of these precontact dogs are largely unknown. We sequenced 71 mitochondrial and 7 nuclear genomes from ancient North American and Siberian dogs from time frames spanning ~9000 years. Our analysis indicates that American dogs were not derived from North American wolves. Instead, American dogs form a monophyletic lineage that likely originated in Siberia and dispersed into the Americas alongside people. After the arrival of Europeans, native American dogs almost completely disappeared, leaving a minimal genetic legacy in modern dog populations. The closest detectable extant lineage to precontact American dogs is the canine transmissible venereal tumor, a contagious cancer clone derived from an individual dog that lived up to 8000 years ago.

Reconstructing Asian faunal introductions to eastern Africa from multi-proxy biomolecular and archaeological datasets

Human-mediated biological exchange has had global social and ecological impacts. In sub-Saharan Africa, several domestic and commensal animals were introduced from Asia in the pre-modern period; however, the timing and nature of these introductions remain contentious. One model supports introduction to the eastern African coast after the mid-first millennium CE, while another posits introduction dating back to 3000 BCE. These distinct scenarios have implications for understanding the emergence of long-distance maritime connectivity, and the ecological and economic impacts of introduced species. Resolution of this longstanding debate requires new efforts, given the lack of well-dated fauna from high-precision excavations, and ambiguous osteomorphological identifications. We analysed faunal remains from 22 eastern African sites spanning a wide geographic and chronological range, and applied biomolecular techniques to confirm identifications of two Asian taxa: domestic chicken (Gallus gallus) and black rat (Rattus rattus). Our approach included ancient DNA (aDNA) analysis aided by BLAST-based bioinformatics, Zooarchaeology by Mass Spectrometry (ZooMS) collagen fingerprinting, and direct AMS (accelerator mass spectrometry) radiocarbon dating. Our results support a late, mid-first millennium CE introduction of these species. We discuss the implications of our findings for models of biological exchange, and emphasize the applicability of our approach to tropical areas with poor bone preservation.

Predicting the viability of archaic human hybrids using a mitochondrial proxy

Ancient DNA evidence has confirmed hybridization between humans and Neanderthals and revealed a complex pattern of admixture between hominin lineages. Many segments of the modern human genome are devoid of Neanderthal ancestry, however, and this non-random distribution has raised questions regarding the frequency and success of hybridisation between ancient human lineages. Here, we examine the hypothesis that hominin hybrid offspring suffered a reduction in fertility by comparing patterns of sequence divergence of mitochondrial and nuclear DNA from numerous hybridising pairs of mammals. Our results reveal a threshold separating species pairs whose divergence values fall within two categories: those whose hybrid offspring can successfully reproduce without backcrossing with their parent species, and those whose hybrid offspring cannot. Using this framework, we predict that the potential hybrid offspring of Neanderthals, Denisovans, the ancient individuals from the Sima de los Huesos and anatomically modern humans would not have suffered a reduction in fertility.

Bridging Archaeology and Genetics

With the development of the polymerase chain reaction (PCR) in the 1980s, the application of molecular methods to archaeological questions has seen a rapid expansion in the last three decades, addressing major research topics including human origins and migrations, domestication and chronology. The recent introduction of next-generation sequencing (NGS) has revolutionised the field, allowing for a larger amount of data to be generated quickly and at ever-decreasing costs. With such techniques now available, it is crucial for a clear and comprehensive dialogue to be established between archaeologists and geneticists. In the following paper, we first review the history of archaeogenetics before addressing some of the major misconceptions that remain commonly widespread across audiences. These include the misconception that genetics can reconstruct full phenotypes or that modern populations can be solely used to retrace a species’ origin or domestication. After exploring the current potential of genetics applied to archaeology through successful case studies, we highlight practical considerations when undertaking archaeogenetic research including sample status and selecting adequate genetic markers and methods. Finally, we suggest ways of bridging the gap between both disciplines so as to allow better collaborations in the future.

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.