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ANIMAL GENETICS |
* Laboratory of Molecular Biology and Animal Breeding, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan 430070, P. R. China and
and
Institute of Criminal Science and Technology, Public Security Bureau of Hu Bei Province, Wuhan 430070, P. R. China
Abstract
To study the genetic diversity of Chinese indigenous pig breeds, a total of 403 pigs from 10 local populations and 1 exotic Duroc breed were genotyped for 20 microsatellite markers. Heterozygosity and Wright’s F-statistics (FIS, FST, and FIT) were calculated to determine the genetic variation in those populations. The observed heterozygosities were in the range of 0.31 (Duroc) to 0.66 (Shengxian). The FIS value was in a range of -0.07 to 0.48. The mean FST showed that approximately 78% of the genetic variation was within-population and 22% was across the populations. The 10 Chinese local breeds were classified into two major groups according to the phylogenetic tree, which was based on standard genetic distance. Four pig populations, Jianli, Ganxi Two Ends Black, Shaziling, and Dongshan were grouped into one branch. Before the study, these four populations were all classified as Central China Two Ends Black according to coat color, shape of the head, and shape of the ear. The Jinhua pig, which also has the two-ends-black coat color, was also grouped to the same branch but was not traditionally classified into this type. The five populations were located in various provinces in central China. The other five populations, Nanyang Black, Hainan Spotted, Huainan Black, Jiaxing Black, and Shengxian Spotted (black body, white feet), were grouped into another branch. The two groups of pig breeds had the same FST value (0.14) when calculated separately. This value was similar to that of Iberian pigs (0.13) but smaller than that of the European pigs (0.27) as reported by other researchers. Our study showed that large genetic differentiation exists in Chinese pig breeds. The grouping of the five two-ends-black populations into one branch of the phylogenetic tree may indicate that the number of conservation farms can be decreased for this type of pig.
Key Words: Chinese Indigenous Population • Genetic Diversity • Microsatellite • Pig
Introduction
China has at least a 7,000-yr history of domesticating pigs (Zhang, 1986
). Over 100 pig breeds, about a third of the world’s pig breeds, exist in China (Li et al., 2000a). They were classified into six types according to their geographic origin, distribution, body conformation, and coat color: I—North China, II—Lower Changjiang Basin, III—Central China, IV—South China, V—Southwest, and VI—Plateau (Zhang, 1986). Each type contains a number of breeds. It will be interesting to examine the genetic relationship among local pig breeds by molecular markers such as microsatellites and to compare them to the traditional classification results.
Microsatellites have been widely used for genetic variation studies in domestic animals. In the pig, genetic diversity studies of some of the commercial breeds and the Chinese Meishan breed were conducted by genotyping multiple microsatellite loci (Johansson et al., 1992; Fredholm et al., 1993; Paszek et al., 1998a,b), and the results showed that the Meishan has a significantly higher mean heterozygosity than the Western breeds (Yorkshire, Hampshire, Duroc, Landrace), as observed at several microsatellite loci (Paszek et al., 1998b). Genetic diversity of some Chinese local breeds investigated by using microsatellites suggested a higher (Li et al., 2000b) or similar (Fan et al., 2002) genetic differentiation among breeds compared with that of Belgian, exotic breeds (British Larger White, Yorkshire, Hampshire), and European breeds (van Zeveren et al., 1995; Kacirek et al., 1998; Laval et al., 2000; Martinez et al., 2000). In this study, we used 20 pairs of microsatellite primers to detect the genetic relationship between 10 local pig populations and to compare two breed-classification methods based on traditional methods or microsatellites.
Materials and Methods
Sample Collection for DNA Analysis
Blood samples were collected from 403 pigs originating from various geographical locations and representing 10 Chinese indigenous populations and 1 exotic breed (Duroc). The distribution of the 10 breeds is shown in Figure 1. Sample size and locality for each population are listed in Table 1. The 10 local breeds are distributed in eight provinces, and the sample size is from 24 to 53. Samples of DNA from two animals from the PiGMaP reference pedigree F1 animals (French 9110010 and 9110012) were also used as controls to identify different alleles.
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; Cassady et al., 2001; Malek et al., 2001). The PCR amplification protocol was a single reaction of 7.5 µL under the following conditions: 0.9 to 1.2 mM MgCl2, 0.1 mM dNTPs, 0.75 µL buffer (10x), 0.2 µM primers (each), genomic DNA 100 ng, and 0.3 U of Taq DNA polymerase. Amplification conditions were as follows: 4 min at 94°C, followed by 30 cycles of 45 s at 94°C, 45 s at 55 to 62°C (depending on the locus), and 45 s at 72°C, followed by an extension of 5 min at 72°C. Fluorescent end-labeled (fluorescent dye: FAM, TET, HEX; the internal size standard; Genescan-TAMAR-500) PCR primers were used, and size characterization of PCR product was performed by an ABI 310 DNA Genetic Analyzer (Applied Biosystems/Perkin Elmer, Foster City, CA).
Data Analysis
To determine the genetic variation within and between breeds, parameters such as heterozygosity and Wright’s F-statistics (FST, FIS, and FIT) were calculated. Heterozygosity is defined as the probability that a given individual randomly selected from a population will be heterozygous at a given locus. The statistic FST is an estimate of variation due to differences among populations, which is the reduction in heterozygosity of a subpopulation due to genetic drift. The statistic FIS is an estimate of variation within populations that measures the reduction in heterozygosity in an individual due to nonrandom mating within its subpopulation. The statistic FIT is the overall inbreeding coefficient of an individual relative to the total population. This includes the contribution due to nonrandom mating within subpopulations (FIS) and that due to population subdivision (FST).
The GENEPOP (Version 3.3) computer package (Raymond and Rousset, 1995) was employed to calculate of the number of alleles, allele frequencies, and the test of Hardy-Weinberg equilibrium. The effective number of alleles was estimated according to Kimura and Crow’s (1994) formula. The Genes in Population (Version 2.0) software (May et al., 1995) was used to analyze observed population heterozygosity (HT), expected heterozygosity (HS), and Wright’s F-statistic at each locus, expected heterozygosity (HE), and observed heterozygosity (HO) in each population. An unweighted pair-group method with arithmetic mean (UPGAM; Sneath and Sokal, 1973) was used to construct the phylogenetic tree based on Nei’s (1972) standard genetic distance using the DISPAN program (Ota, 1993) and PHLIP 3.57c software package (Felsenstein, 1993). Simple allele sharing statistics (Bowcock et al., 1994) were applied to analyze the genetic structure of the breeds.
Results
Allele Frequencies, Heterozygosity, and F-Statistics
Allele frequencies are available from the corresponding author upon request. Microsatellite allele sizes observed in these 11 breeds, published allele sizes, observed heterozygosity (HS), expected heterozygosity (HT), Wright’s F-statistics (FIS, FIS, and FST) at each locus, and the number of populations deviating from Hardy-Weinberg equilibrium (HWE) are all shown in Table 2. In this study, all loci were polymorphic and the number of alleles per locus varied from 13 to 35, which indicates that the microsatellites used are suitable for genetic diversity analysis. Private alleles were present in all populations (e.g., some alleles in some loci can only be found in one population). Mean observed heterozygosities (HO), mean expected heterozygosities (HE), mean polymorphic information (PI) content, and a measure of the allelic diversity at a locus was estimated for each of the polymorphic loci (Botstein et al., 1980), as well as the mean observed number of alleles and the mean effective number of alleles for all populations (Table 1
). Although varying among populations, the observed mean heterozygosity was lower than the expected mean heterozygosity for all populations. Measures of genetic variation for each population showed significant differences (P < 0.001, data not shown) for multilocus heterozygosity among breeds, and the level of genetic variation within the population of Hainan Spotted (HE = 0.77) was the highest and that of Duroc (HE = 0.47) was the lowest.
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. The HT varied from 0.51 (SW2439 and PYDN) to 0.88 (S0107). The FST per locus varied from 0.05 (S0107) to 0.37 (SW1678), and the average FST of all loci was 0.22. Multilocus FST values indicated that around 22% of the total genetic variation was explained by population differences, with the remaining 78% corresponding to differences among individuals within population. The average FST value of the two-ends-black genetic group is the same as the black and spotted group (0.14) when calculated separately (see below, in Table 4). The HWE test showed that all loci deviated from HWE when analyzed across populations. These deviations are likely caused by the small effective population sizes and the difficulties in collecting enough unrelated individuals.
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standard genetic distance of the 11 porcine populations is listed in Table 3. The UPGAM tree (Figure 2) was constructed based on the standard genetic distance. The numbers at the nodes are values for 1,000 bootstrap resamplings of the 20 genotyped loci. The bootstrap values obtained in the UPGAM tree at the nodes suggest that the tree is fairly robust.
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Genetic Diversity
Genetic diversity can be evaluated by the number of alleles by locus, average number of alleles for all loci, heterozygosity, and PI content. In total, 496 alleles were found at the 20 loci across the 11 breeds in this study. The average number of alleles found by locus, considering all populations, was 24.8. Barker (1994) suggested that microsatellite loci used in studies of genetic distance should have no fewer than four alleles in order to reduce the standard errors of distance estimates; thus, the microsatellites used in this study were suitable for genetic diversity analysis. More alleles were found at each locus in this study as compared to reports from other researchers (Table 2), and the range in size of the alleles was extended because of the larger effective population size in this study. At least one allele at each locus in Rohrer et al. (1994) was detected in Jiaxing Black pigs in this study. This might be due to Meishan and Fengjing pigs used in the Rohrer et al. (1994) reference family and the Jiaxing Black pigs in our study all being subpopulations of Taihu pigs.
Takezaki and Nei (1996) determined that, for markers to be useful for measuring genetic variation, they should have an average heterozygosity of between 0.3 and 0.8 in the population. The range of heterozygosity of the markers in the 10 local populations in this study was between 0.46 and 0.66, and therefore the markers were appropriate for measuring genetic variation. Although varying among populations, observed mean heterozygosity was lower than the expected mean heterozygosity for all the populations. All loci deviated from HWE in at least four populations (P < 0.01). Three loci (S0076, SW2435, S0107) had an excess of homozygotes in all of the populations. There were 9 to 18 loci in each population that deviated from HWE. The high levels of heterozygosity in all the breeds in this study may be due to low selection pressure in the indigenous Chinese breeds.
Botstein et al. (1980) developed the PI content value for the measurement of a marker’s informativeness in a linkage analysis of a rare dominant disease. The usefulness of a marker in a model-based linkage analysis depends on its degree of polymorphism. Codominant markers are now also used in linkage studies, as well as in some genetic variation studies. The mean PI content in different local populations in this study was between 0.53 and 0.74, with Jinhua the lowest and Hainan Spotted the highest. The low PI content of Jinhua may be due to the higher selection pressure in this breed to produce the well-known "Jinhua ham."
Genetic Relationships
The standard genetic distances are listed in Table 3. Breeds having the same phenotype were grouped into one branch in this study (Figure 2). Jianli pigs in the Hubei province, Ganxi Two-Ends-Black in the Jiangxi province, Shaziling in the Hunan province, and Dongshan in the Guangxi province—all Central China type pigs—were amalgamated into one breed traditionally called the Central China Two Ends Black type (Zhang, 1986). These four populations have similar phenotypic characteristics, such as black color at the two ends (i.e., black color on the head and buttocks) with a wide white belt in the middle of the body and a similar shape of the head and ear. However, the Jinhua breed in Zhejiang province, which has a phenotype similar to that of these four breeds (some pigs have a small bunch of white hair on the center of forehead, and some pigs have a white hair belt from head to nose) but had not traditionally been classified (Zhang, 1986) into this breed, was also grouped to the same branch. The bootstrap values of 1,000 replicates were high, indicating that the 20 microsatellite loci were suitable for the genetic relationship analysis, and also agreeing with the theory that the breeds should be categorized by their phenotype instead of geographic location. The other five breeds in this study are black or white—black spotted pigs. Among them, the Shaziling was not first grouped with Jiaxing Black, which is located near it, but was first grouped with Nanyang Black, and then grouped together with Jiaxing Black. The Huainan Black breed was grouped with Hainan Spotted, which is geographically located far away. According to the formula D = 2vt, where D is genetic distance, v is 2.0 x 10-4 mutations per locus per generation, and t is the time measured in generations after divergence of populations (Takezaki and Nei, 1996; Cavalli-Sforza, 1998; Nichols et al., 2001), the time for the divergence of these two populations (Huainan Black and Hainan Spotted, genetic distance: 0.37, 95% confidential interval = 0.35 to 0.53) was 970 yr ago (95% confidential interval is 924 to 1,321 yr). One possible reason for these two breeds being grouped together may be that Huaninan Black might be one of the founders in the breeding history of Hainan Spotted due to the transportation of pigs accompanying the migration of people from the middle part of the mainland to the seaside according to historical records.
The mean FST value indicates that only about 22% of the total genetic variation can be attributed to the differentiation between populations and 78% within populations. The isolation of the two genetic groups from each other indicates there were low levels of gene exchange during breed formation in those Chinese indigenous pigs. A comparison of observed heterozygosity and F-statistic values obtained in this study with some other previously reported breeds is listed in Table 4. The mean FST value (0.14) in this study is lower than that of other Chinese local populations (0.18; Fan et al., 2002) and European breeds (0.27; Laval et al., 2000), but higher than that of Iberia pigs (0.13; Martinez et al., 2000) and Mexican pigs (0.11; Lemus-Flores et al., 2001). The range of observed heterozygosity in our study is also similar to that of other studies (Table 4). Higher FIS values were observed in the Chinese local and Mexican hairless pigs than in the European pigs. This could be the result of inbreeding. However, FIS measures how much excess (or reduction of) heterozygosity exists between the observed and expected heterozygosities (e.g., FIS = (HE - HO)/HE, where HE = expected heterozygosity and HO = observed heterozygosity) in a population. In our study, no populations were in Hardy-Weinberg equilibrium, and there was an excess of homozygotes. Thus, the expected heterozygosity is higher than that observed for all breeds, and the FIS values are positive. Two factors may cause the high heterozygosity observed in our study: the low rate of selection pressure because of the lack of improvement programs and the fact that different genetic lineages exist within breeds. The latter factor is called the Walhund effect. This effect is a result of isolated subpopulations existing within a breed and causing the concomitant excess of homozygotes within the subpopulations. But when these subpopulations are joined together in one breed, a high heterozygosity is observed at the breed level.
This study showed that microsatellite loci are useful markers for studying the genetic variation between these 10 Chinese pig populations. Three breeds—Jinhua, Shengxian Spotted, and Jiaxing Black—are all from the Zhejiang province, but did not show the closest relationship according to the phylogenetic tree. Each of them was grouped with breeds from other provinces first. For example, Jinhua was grouped together with the four populations of the Central China Two Ends Black type. The Shengxian Spotted White-Black and Jiaxing Black were grouped together with the spotted pigs or black pigs from the other provinces first. This interesting result agreed with the traditional classification proposed earlier by some experts (Zhang, 1986), which indicates that breed classification should rely on the phenotype first, rather than geographic location. The present study contributes to the knowledge of the genetic structure and molecular characterization of the Chinese local pig breeds. Most of the pig populations in this study have a conservation farm under the government’s support at the present time. The traditional classification and the results from this study suggest combining some breeds into one group for conservation to reduce the cost. For example, combining the Dongshan and Shaziling into one group, Shengxian Spotted and Manyang Black into one group, and a cross between the combined breeds can be utilized to enhance the heterozygosity.
Implications
These results demonstrated that the 20 microsatellites used in this study were useful markers to study genetic diversity among 10 Chinese local pig breeds. The closest breeds in the phylogenetic tree had similar phenotypes but were not geographically close. This may offer useful information for further classifying the local breeds in China based on phenotype and molecular characterization.
Footnotes
1 This work was supported by National Key Projects for Basic Research and Development Plans of China (G2000016103), National High Technology and Science Development Plan of China (863), National Outstanding Youth Science Foundation of China (39925027), EU-China Collaboration Project (QLRT-2001-01059), and 863 Project (2001AA222241). We thank the USDA-supported U.S. Pig Genome Coordination Project for the contribution of the primers (courtesy of M. F. Rothschild) and thank D. Milan (INRA, France) for providing the control animal DNA. We also thank Z. Z. Peng for suggestions, X. L. Wu for help with data analysis, and J. McElroy for editing. 
2 Correspondence: Shizishan St. (phone: 86-27-87281306; fax: 86-27-87280408; e-mail: lkxblghi{at}public.wh.hb.cn).
Received for publication October 17, 2002. Accepted for publication September 23, 2003.
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