Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA

Abstract

The establishment of agricultural economies based upon domestic animals began independently in many parts of the world and led to both increases in human population size and the migration of people carrying domestic plants and animals. The precise circumstances of the earliest phases of these events remain mysterious given their antiquity and the fact that subsequent waves of migrants have often replaced the first. Through the use of more than 1,500 modern (including 151 previously uncharacterized specimens) and 18 ancient (representing six East Asian archeological sites) pig (Sus scrofa) DNA sequences sampled across East Asia, we provide evidence for the long-term genetic continuity between modern and ancient Chinese domestic pigs. Although the Chinese case for independent pig domestication is supported by both genetic and archaeological evidence, we discuss five additional (and possibly) independent domestications of indigenous wild boar populations: one in India, three in peninsular Southeast Asia, and one off the coast of Taiwan. Collectively, we refer to these instances as "cryptic domestication," given the current lack of corroborating archaeological evidence. In addition, we demonstrate the existence of numerous populations of genetically distinct and widespread wild boar populations that have not contributed maternal genetic material to modern domestic stocks. The overall findings provide the most complete picture yet of pig evolution and domestication in East Asia, and generate testable hypotheses regarding the development and spread of early farmers in the Far East.

Fig. 1.

A map of East Asia showing modern political and Chinese and Indian province boundaries, and a phylogenetic tree depicting the relationships between clades of wild and domestic pigs in the region. Colored circles within each Chinese or Indian province, each country (other than China or India), and each island indicate the presence of at least a single sample belonging to the colored regions on the tree below. Each of the 13 individual clades made up solely of wild boar are colored green on both the tree and the map. The numbers below the clades represent the posterior probability support values. The branch leading to the unique Lanyu pig haplotype is labeled on the tree, and the word Lanyu is placed on the map. Four additional clades, labeled MC1–MC4 and colored blue, purple, brown, and orange, respectively, possess both regionally restricted wild boar populations and domestic pigs (Fig. S3). The left-hand side of the tree is a polytomious cluster made up of individual branches of both wild and domestic pigs (and nine clades made up solely of domestic pigs) collectively referred to as the general cluster and colored gray. The two sides of the tree are separated by a dashed black line also shown in Fig. 2. Specific location information for each sample can be found in Tables S1–S5 and Figs. S1–S3. The Indus, Ganges, Yellow, and Yangtze Rivers are highlighted in blue. The inset on the bottom left of the map shows the locations and relative ages of the archaeological sites from which the ancient pig bones were retrieved, and the numbers 1–6 correspond to the sites Gaohong, Taosi, Guchengzhai, Wangchenggang, Wadian, and Jiahu, respectively.

Fig. 2.

Two median-joining networks in which node sizes are proportional to haplotype frequencies depicting (A) the relationships among 1,540 modern wild and domestic samples in a 378-bp alignment and (B) the relative position of the ancient haplotypes after the archeological samples were added to a reduced 185-bp alignment. Wild, domestic, and ancient samples are shown in black, white, and red, respectively, and asterisks also mark the positions of the ancient samples. Inferred haplotypes are represented by small orange dots. The relative position of the Lanyu pig and mutations along the branches are shown in Fig. S2. The dashed black line dividing the networks correlates with the line shown in Fig. 1 demonstrating the consistent distinction between the general cluster and the wild and mixed haplotypes.