The Consequences of Gene Flow between Wild and Domestic Populations during Livestock Evolution

Lead Research Organisation: University of Oxford
Department Name: School of Archaeology

Abstract

Generally speaking, modern domestic species are actively prevented from interbreeding with wild populations. The few exceptions to this rule involve the deliberate generation of novel hybrid pets such as those involving domestic and wild cat species. This practice of incorporating wild species in breeding lines is strongly discouraged amongst livestock species since the introduction of genes from wild populations reduces productivity and the degree of tameness in the hybrids. In the recent past, however, husbandry practices were far less restrictive. Recent ethnographic and genetic analyses have revealed that interbreeding between numerous species of domestic and wild species was, in fact, the rule and not a rare exception.

While gene flow from wild populations can be detrimental, it can also have a positive impact on livestock populations. For example, by decreasing the risks associated with inbreeding and by introducing genetic variation that allowed for rapid adaptation to novel environments. Adaptive gene flow therefore potentially played an important role during the spread of domestic animals across the world. This is especially true of pigs since geographically and genetically differentiated populations of wild boar are present across Eurasia and adapted to a wide variety of climates and environments; thus providing raw material that could have been absorbed by arriving domestic pigs. In fact, we demonstrated that gene flow between wild and domestic pigs was common and that it began immediately following the introduction of pigs to Europe from the Near East where they were initially domesticated.

Despite this gene flow, pigs in Europe maintained their integrity as domestic animals by retaining their morphological and behavioural distinctiveness, suggesting that though some wild boar genomic variation was incorporated into domestic stocks, many wild boar genetic variants were actively expunged. Here, we will determine whether some wild genetic variants were preferentially expunged and whether some were preferentially incorporated into domestic populations. Ultimately, this project will reveal not only the genomic basis for domestication, but also how domestic pigs adapted to novel environments, by identifying specific genomic regions that were rapidly incorporated, and which ones were resisted during gene flow.

To do so, we will assess the DNA preservation of more than 1,000 ancient pigs and wild boar from Eastern and Western Eurasia over the past 10,000 years, and then sequence the entire genomes of the best preserved specimens. Armed with this data, we will establish the spatial and temporal differences in the proportion and genomic location of the incorporation of wild boar genes into domestic stocks. The results will allow not only an unprecedented understanding of the origins of domestic animals, they will also have important ramifications for the conservation of endangered wild boar populations and for pig breeders and consumers of pork for whom the authenticity of domestic and wild meat is crucial.

Planned Impact

The results of this project will be of interest to, and directly benefit, numerous beneficiaries in the UK and worldwide including: 1) Members of the public, consumer unions and welfare groups, 2) Farmers and breeders, and 3) Conservation agency and policy makers.

Members of the public, consumer unions and welfare groups
By studying the origin of domestic pigs and their relationships with wild boar from the Neolithic to the present, this study will generate insights into the biological and cultural origins of modern society. Our results will generate significant public interest since domestic animals play a vital role in our daily lives. The public is also fascinated with human origins and our work will lead to a greater understanding of how modern society originated and how human selection has affected animals through artificial selection. To take advantage of this demonstrated appetite, we will leverage our experience with the media, having taken part in a range of TV and Radio broadcasts featuring our domestication research including BBC1 and 2, Radio 4, German ZDF, National Geographic and the Discovery Channel, to promote our findings. More practically, our research will provide consumer unions and welfare groups with the means to better assess genetic methods currently used for assessing the authenticity of meat products, particularly those from wild boar.

Farmers and breeders
Our project will provide insights relevant to both breeders and farmers regarding how pig husbandry has changed through time. In particular, our research will provide the opportunity to assess whether genetic diversity in pigs has decreased in the recent past due to modern breeding practices (e.g. quantitative genetics and genomic selection). We will also reveal the role that wild boar have played during the domestication and subsequent dispersal of pigs and how important local populations of wild boar have been in allowing incoming domestic pigs to adapt to new environments. In addition, our study will also provide novel insights into past husbandry practices that will be relevant for modern farmers and breeders.

Conservation agencies and policy makers
This research will allow the current single species status of S. scrofa by the IUCN Red List to be analysed and our results will inform conservations strategies in for example, the rare Ryukyu pig, S. s. riukiuanus (Japan) and isolated populations of the Mediterranean S. s. baeticus. In addition, we will assess the status of U.K. wild boar which are thought to have gone extinct within the last 1,000 years. The Department for Environmental and Rural Affairs consider wild populations "feral" (i.e. mostly escaped farm animals) yet we do not know the contribution (if any) of native wild boar to the modern domestic pig gene pool. Identifying the potential presence of prehistoric genetic elements preserved in the specific U.K. breeds will inform both management strategies and government livestock policy.

The conservation of rare livestock breeds will also be influenced by our study. The 130 breeds currently listed as endangered by the Food and Agriculture Organisation (UN) represent an important cultural heritage and reservoir of genetic variation. By assessing the patterns of gene flow from local wild populations (including extinct populations such as the UK) into rare breeds, we will test the hypothesis that these populations retain genetic variations linked to local wild boar populations and adaptation to local environments. These insights will be crucial to promote awareness and conservation both in the UK (through the Rare Breed Conservation Trust) and worldwide (through the Livestock Conservancy).

Publications

10 25 50
publication icon
Frantz LAF (2019) Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe. in Proceedings of the National Academy of Sciences of the United States of America

publication icon
Frantz LAF (2020) Animal domestication in the era of ancient genomics. in Nature reviews. Genetics

publication icon
Sinding MS (2020) Arctic-adapted dogs emerged at the Pleistocene-Holocene transition. in Science (New York, N.Y.)

publication icon
Lord KA (2020) The History of Farm Foxes Undermines the Animal Domestication Syndrome. in Trends in ecology & evolution