Levels of genetic diversity and the structuring of geographic populations provide important clues to local adaptation and species evolution. Such information can further be employed to understand the effect of genetic variation of regional wild boars on pig domestication in East Asia and to facilitate conservation and management of this species at a regional scale. In this study, wild boar populations from East Asia showed various levels of genetic diversity, as well as a distinct genetic structure, related to geographic distribution.
Genetic diversity and population structure of wild boar in East Asia
The pattern and magnitude of allelic diversity vary with the geographic distribution of wild boars in East Asia. Wild boars from southeastern regions, represented by Yunnan province of China, Vietnam and Indonesia, exhibited generally high levels of genetic diversity with large numbers of alleles. In contrast, relatively low levels of genetic diversity were found in wild boars from Northeast Asia, except Primorsky Krai, Russia which has an intermediate level of allelic diversity.
The high level of genetic diversity and large numbers of alleles in wild boars from Southeast Asia are expected given the historical geographic range of S. scrofa. Previous studies
[3, 12, 14] revealed that S. scrofa originated from Islands of Southeast Asia, i.e. an “ISEA” origin of wild boar. Although various factors such as climatic fluctuations and human-mediated translocations can affect the genetic composition of a spreading species, its gene pool will be retained with a higher probability in the area of origin than in areas of colonization. Additionally, extensive inter-specific gene flow in the genus Sus took place during glacial periods when a land bridge formed between the islands of Southeast Asia
, and this could explain the observed high level of genetic diversity in ISEA.
Structure analysis using the hierarchical island model revealed that Indonesian wild boars are differentiated from other populations of Southeastern Asia, despite some individuals with genetic profiles similar to those of wild boars from Yunnan province and Vietnam (Figures
3). In addition, the high proportion of private alleles and high allelic diversity in the Indonesian wild boar population support its subspecific classification as the “Indonesian race”, S. s. vittatus, proposed by Groves and Grubb
In contrast, wild boars from most of mainland Korea and Jeju Island had genetic diversity almost two fold lower than wild boars from Southeast Asia. The wild boar population from Jeju Island (H
E = 0.549; Ar = 3.1) exhibited the lowest genetic diversity among all populations sampled from East Asia. Negligible gene flow from the Korean mainland (mean Nm = 0.764, Table
2), and the sudden population increase on Jeju Island during recent decades, could account for the low level of genetic diversity on the island, and suggest there has not been enough time to reach mutation/migration-drift equilibrium since human-mediated translocation or natural migration.
Patterns of genetic diversity and differentiation at local and regional scales observed in this study, together with results from the model-based structure analysis, suggest that wild boars in Northeast Asia share closer ancestry with wild boars in southern China than do those in Vietnam and Indonesia, indicating gradual gene flow from ISEA through Southern China (Figure
2). A diverging gene pool and high level of genetic diversity in wild boars from East Asia are likely reflected in a high diversity of local pig breeds in Asia, arising during multiple and independent domestication events in this region
In contrast to a previous study based on mtDNA and nuclear genes
, which found no genetic structure among wild boar populations in East Asia, we found high genetic variation and differentiation between wild boar populations at both local and regional levels. Mitochondrial DNA sequence comparisons indicated that genetic clusters of wild boars from East Asia, including China, Korea, Japan and the Russian Far East, were not clearly separated by region
. In addition, no conspicuous genetic structure in East Asia, including China, Korea and Japan, was detected based on three different marker systems, mtDNA, microsatellite and Y-chromosome genes
. In these cases, the number of samples and markers used for wild boar study in East Asia probably were not enough to detect population structure. Alternatively, the use of populations such as domestic pigs with strong geographic structuring could mask the hidden structure of wild boars in East Asia that might otherwise exist in such region. Our contrasting results relative to previous studies
[10, 11, 17] could also be due to the use of different marker systems. Although both mtDNA and microsatellite loci analyses showed indication of population structuring in European wild boars
[18–20], microsatellite loci have shown better resolution in detecting genetic structure among geographic populations than mtDNA
. Population differentiation and admixture in the recent past can be better detected by fast-evolving markers like microsatellites.
Geographical distance was significantly correlated with genetic distance when the unique Jeju population was excluded (Additional file
1: Figure S2). A hierarchical genetic differentiation related to geographical distances is also well-supported by the AMOVA incorporating three regions (Table
3). Furthermore, Principal Coordinates Analysis (PCA) showed the wild boar populations in East Asia occupied unique positions along PC 1, mainly related to geographic distribution. Taken together, our data indicate that genetic differentiation of wild boars in East Asia is maintained by geographic separation.
Genetic status of local wild boar populations in South Korea
Archaeological evidence suggests that wild boars appeared on the Korean peninsula in the mid-Pleistocene, ca. 780,000 to 130,000 years before present
. However, predators, such as wolf and tiger, which have played important roles in effectively controlling the population size of wild boar, have been absent from South Korea over recent decades. As a result, wild boar is the largest mammal with an extensive distribution in South Korea, although Asiatic black bears (Ursus thibetanus) were reintroduced to the mainland a decade ago
. Archaeological evidence and ancient records indicate that wild boars became established on Jeju Island, the largest island in southern Korea, presumably between the 1st and 8th centuries A.D.
[23, 24]. Modern populations decreased and went undetected for several decades, but over the last decade, wild boars have greatly increased on the island. Although the reason for the recent increase of wild boars on Jeju Island is unclear, it has been assumed that some captive individuals escaped to the wild. As a consequence of wild boar population growth on the mainland and Jeju Island in South Korea, proper management of the species is of increasing concern, and population genetics would be a useful tool to reveal whether gene flow occurs between local wild boar populations.
Structure analysis (K = 7) showed that wild boars from mainland Korea are represented by two genetic clusters (Figures
3). Although genetic traits within populations in mainland Korea were not clearly discrete, genetic profiles were gradually displaced from the north-central region (KGGW and KGWW) to the southeast region (KGSW), followed by the southwest region (KJLW) (Figure
2). Pairwise F
ST and gene flow estimates (Nm) support a gradual cline in genetic structure in mainland Korea (Table
2). These three regions of the Korean peninsula are geographically separated by the Baekdu-daegan mountain range, which runs most of the length of the eastern peninsula, from Baekdu Mountain in the north to Jiri Mountain in the mid-south. This mountain range may function as a geographical barrier to wild boar dispersal, although they are capable of crossing mountain ridges. Moreover, S. scrofa does not tend to disperse long distances from their birth site, with geographic ranges less than 6.5 Km2
Our result showed that Jeju wild boar had a closer relationship with Yunnan rather than the mainland Korea, which suggests that wild boars in Jeju Island share closer common ancestry with wild boars in Yunnan, China than mainland Korea. This is in agreement with the conclusion of a previous study that Jeju Island wild boars probably introduced from somewhere in China
, and were not directly originated from mainland Korea. A phylogenetic study using mitochondrial sequences suggested that wild boar from Jeju Island should be allocated to the Chinese wild boar cluster
. However, precise identification of the geographic origin of the Jeju Island wild boar will require a survey of more samples from broadly spaced regions using a variety of analytical methods, such as paternal history using Y-chromosome genes and maternal history using mitochondrial DNA.
For effective management of wild boars in Korea, genetic traits must be considered to establish appropriate strategies. Our results show that wild boar populations on mainland Korea are genetically structured. For example, wild boars from Jeolla-do, in the southwest region of South Korea, shared only 3.6% genetic composition with the population from Gyeonggi-do in the northwest. This result indicates that wild boar distribution and partial isolation in the Korean peninsula are possibly maintained by geographic barriers such as mountain ridges, lowlands and islands. Although wild boars are now abundant in South Korea, various levels of genetic and ecological studies will be required to obtain adequate information for long-term management.