Genomic history of early dogs in Europe | Nature

Download PDF

Subjects

- Archaeology

- Evolutionary biology

- Evolutionary genetics

- Genomics

- Population genetics

Abstract

The earliest morphologically identifiable dogs are from Europe and date to at least 14,000 years ago1,2,3,4,5, although early remains are also found in other regions. The origin of early dogs in Europe, and their relationships to other dogs, has remained elusive in the absence of genome-wide data. Similarly, although dogs were the only domestic animal to predate agriculture, little is known about how the arrival of Neolithic farmers from Southwest Asia affected the dogs living with European Mesolithic hunter-gatherers. Here we analysed 216 canid remains, including 181 from Palaeolithic and Mesolithic Europe. We developed a genome-wide capture approach that enriched endogenous DNA by 10–100-fold and could distinguish dog from wolf ancestry for 141 of 216 remains. The oldest dog data that we recovered are from a 14,200-year-old dog from the Kesslerloch site in Switzerland, and we find that it shares ancestry with later worldwide dogs—inconsistent with the hypothesis that European Upper Palaeolithic dogs derived wholly from a separate domestication process. The Kesslerloch dog already displays more affinity to Mesolithic, Neolithic and present-day European dogs than to Asian dogs, demonstrating that dog genetic diversification had started well before 14,200 years ago. We find a Neolithic influx of Southwest Asian ancestry into Europe, but this seems to have been of smaller magnitude than in humans, suggesting that Mesolithic dogs contributed substantially to Neolithic, and, ultimately, probably also modern, European dogs.

Main

Dogs (Canis lupus familiaris) were domesticated from grey wolves (Canis lupus) towards the end of the last Ice Age, and were the first animals to enter into a domestic relationship with humans. Where in the world this happened, and which human group or groups were involved in the process of domestication, remains unknown6,7,8,9,10,11,12,13,14. The earliest known canid remains with probable dog morphology have been found in Europe, and include remains from the Bonn–Oberkassel2, Kesslerloch1, Le Morin3, Errala4 and Paglicci5 sites, all from the period 14,000–17,000 years ago (14–17 ka); however, putative dog remains within a few thousand years younger than these have also been found in East Asia15, the Levant16 and the Americas17, such that the archaeological record does not clearly point to any particular geographical region as the centre of domestication. Some much earlier remains have also been hypothesized to be dogs, but many morphological assignments remain contested in the absence of genetic data18.

Despite Europe having the earliest archaeological evidence of dogs, European wolves that lived during the Late Glacial period (~23–12 ka), when dogs probably arose, have not been found to have contributed detectably to dog ancestry14. Instead, dogs overall show stronger genetic affinities to Late Glacial wolves from eastern Eurasia14. But further to this, dogs exhibit some degree of variation in their genetic relationships to ancient wolves, implying a ‘dual ancestry’ model in which at least two distinct wolf populations must have contributed ancestry to dogs14. In particular, dogs in Southwest Asia and Africa show an affinity to wolves in Southwest Asia, suggesting a second source from there14. The identities of the wolf source populations, whether they imply a single or multiple domestication processes, and their relationships to the earliest dogs in Europe, remain undetermined.

With the exception of Mesolithic dogs from Karelia in northeastern Europe13,19, previous genome-wide analyses of European dogs have been restricted to the Neolithic period and later8,12,13. DNA analyses of older putative dogs have been restricted to mitochondrial DNA, which does not always reliably distinguish wolves from dogs10. Neolithic and later European dogs have been found to be genetically intermediate between East Eurasian dogs on the one hand, and Southwest Asian and African dogs on the other13. The genomic ancestry of dogs in Europe predating the Neolithic, in the Upper Palaeolithic and Mesolithic periods—including the probable dog remains dating to 14–17 ka—remains unknown. It is also unknown how the Neolithic transition, which involved large-scale migrations of people and domestic animals into Europe from Southwest Asia, affected the dog populations already present in Europe during the Mesolithic.

Targeted genome-wide DNA enrichment

We extracted and analysed DNA from 216 canid skeletal remains (Supplementary Data 1), at least 181 of which come from pre-Neolithic contexts in Europe (Fig. 1a). Some of these remains might derive from the same biological individual (Supplementary Data 5). Our sampling included remains from the Kesslerloch site, Switzerland (14.2 ka, Magdalenian culture, n = 104), the Gnirshöhle site, Germany (~15 ka, Magdalenian, n = 35), Goyet and v