Angela R. Perri

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.

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.

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.

Hunting dogs as environmental adaptations in Jōmon Japan

Abstract Was the use of hunting dogs an adaptation to the post-glacial deciduous forest environment in the northern temperate zone? Dog burials in Jōmon Japan appear closely associated with a specific environment and with a related subsistence economy involving the hunting of forest ungulates such as sika deer and wild boar. Dogs were valued as important hunting technology, able to track and retrieve wounded animals in difficult, forested environments, or holding them until the hunter made the final kill. Greater numbers of dog burials during the later Jōmon phases may reflect a growing dependence on hunting dogs to extract ungulate prey from forests in an increasingly resource-strained seasonal environment.

New Evidence of the Earliest Domestic Dogs in the Americas

The domestication of dogs probably occurred in Eurasia by 16,000 years ago, with the initial peopling of the Americas potentially happening around the same time. Dogs were long thought to have accompanied the first migrations into the Americas, but conclusive evidence for Paleoindian dogs is lacking. The direct dating of two dogs from the Koster site (Greene Co., Illinois) and a newly-described dog from the Stilwell II site (Pike Co., Illinois) to between 10,190-9,630 cal BP represents the earliest evidence of domestic dogs in the Americas and individual dog burials in worldwide archaeological record. The over 4,500 year discrepancy between the timing of initial human migration into the Americas and the earliest evidence for domesticated dogs suggests either earlier dogs are going unseen or unidentified or dogs arrived later with a subsequent human migration.

Paleogenomic Inferences of Dog Domestication

Domestication is the result of a complex interplay of both biological and cultural processes. The mechanism underlying today’s variety of domesticates has long sparked the interest of researchers but has always been difficult to define. While dogs (Canis familiaris) are now firmly established as the earliest domesticated animal, most questions about their domestication are still unresolved, including the location, the timing, and the potential drivers of domestication. Genetic evidence accumulated over the last 20 years unequivocally identified Canis lupus—a gray wolf—as the species giving rise to all modern dogs and suggested locations including Eastern Asia, Central Asia, the Middle East, and Europe as potential domestication origins. Inferences about the timing of dog domestication are equally controversial. A date in the latest Upper Paleolithic, between 15,000 and 12,000 years ago, has long been the accepted timing of domestication due to clear archaeological evidence of morphologically distinct modern dogs by this time, and more recent genetic findings have confirmed the onset of dog domestication in the Late Pleistocene. In order to disentangle the complexity and thus derive a comprehensive understanding of dog domestication, we need to develop evolutionary models that include all available evidence from archaeology, morphology, and genetics. While time travel is still fiction and studying domestication at the moment of action impossible, paleogenomic approaches provide intriguing prospects and necessary means to decipher the many facets of domestication and deliver such evidence. Consequently, recent paleogenomic work has proposed a dual domestication process in Europe and Eastern Asia, which might be a first step toward reconciling some of the previous divergent conclusions.

Earliest Evidence of Toxocara sp. in a 1.2-Million-Yr-Old Extinct Hyena (Pachycrocuta brevirostris) Coprolite from Northwest Pakistan

Abstract The study of fossil parasites can provide insight into the antiquity of host–parasite relationships and the origins and evolution of these paleoparasites. Here, a coprolite (fossilized feces) from the 1.2-million-yr-old paleontological site of Haro River Quarry in northwestern Pakistan was analyzed for paleoparasites. Micromorphological thin sectioning and Fourier-transform infrared spectrometry (FTIR) analysis confirms the coprolite belonged to a bone-eating carnivore, likely the extinct giant short-faced hyena (Pachycrocuta brevirostris). Parasitological analysis shows the coprolite to be positive for Toxocara sp. To our knowledge, this is the earliest evidence for Toxocara sp. found.

A bobcat burial and other reported intentional animal burials from Illinois Hopewell Mounds

Abstract The Elizabeth site is a bluff-top mortuary mound group constructed and primarily used during Hopewellian (Middle Woodland) times. Recent reanalysis of nonhuman skeletal remains from the site reveals that an intentional burial previously identified as a dog (Canis familiaris) is actually an immature bobcat (Lynx rufus). As a result of this discovery, we reevaluated eight other purported animal burials from Illinois Middle Woodland mounds, including seven dogs and a roseate spoonbill (Platalea ajaja). The dogs all appear to be intrusive or unrelated burial events, but both the bobcat and the roseate spoonbill were definite Hopewellian mortuary interments. The roseate spoonbill was decapitated and placed beside a double human burial. But the bobcat was a separate, human-like interment wearing a necklace of shell beads and effigy bear canine teeth (Figures FIGURE 1 and FIGURE 2). To our knowledge, this is the only decorated wild cat burial in the archaeological record. It provides compelling evidence for a complex relationship between felids and humans in the prehistoric Americas, including possible taming.

Modern wolves trace their origin to a late Pleistocene expansion from Beringia

Grey wolves (Canis lupus) are one of the few large terrestrial carnivores that maintained a wide geographic distribution across the Northern Hemisphere throughout the Pleistocene and Holocene. Recent genetic studies have suggested that, despite this continuous presence, major demographic changes occurred in wolf populations between the late Pleistocene and early Holocene, and that extant wolves trace their ancestry to a single late Pleistocene population. Both the geographic origin of this ancestral population and how it became widespread remain a mystery. Here we analyzed a large dataset of novel modern and ancient mitochondrial wolf genomes, spanning the last 50,000 years, using a spatially and temporally explicit modeling framework to show that contemporary wolf populations across the globe trace their ancestry to an expansion from Beringia at the end of the Last Glacial Maximum - a process most likely driven by the significant ecological changes that occurred across the Northern Hemisphere during this period. This study provides direct ancient genetic evidence that long-range migration has played an important role in the population history of a large carnivore and provides an insight into how wolves survived the wave of megafaunal extinctions at the end of the last glaciation. Moreover, because late Pleistocene grey wolves were the likely source from which all modern dogs trace their origins, the demographic history described in this study has fundamental implications for understanding the geographical origin of the dog.