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. 2024 Oct 5;103(12):104383. doi: 10.1016/j.psj.2024.104383

Analysis of genetic diversity and genetic structure of indigenous chicken populations in Guizhou province based on genome-wide single nucleotide polymorphism markers

Sheng Wu ⁎, Zhiwen Chen *, Xiaohong Zhou *, Juanhong Lu *, Yingping Tian *, Yaozhou Jiang *, Qinsong Liu *, Zhong Wang *, Hui Li *, Lujiang Qu †, Fuping Zhang *,1
PMCID: PMC11539430  PMID: 39447329

Abstract

Guizhou province in China is rich in indigenous chicken breeds, playing an essential role in the genetic improvement of modern chickens. Genetic diversity has decreased in recent decades due to accelerated breeding processes and changing conservation priorities. To determine the genetic diversity and population structure of Guizhou indigenous chicken breeds, we used 55K genotyping arrays to conduct population genetic analysis on 233 individuals from 8 Guizhou indigenous breeds and 263 individuals from 9 Guizhou indigenous chicken populations. We evaluated the genetic diversity parameter (heterozygosity, proportion of polymorphic markers, and nucleotide diversity), linkage disequilibrium (LD), population structure, and genetic differentiation (FST and genetics distance). Genetic diversity results indicated that the genetic diversity of chicken breeds in Guizhou province is relatively affluent. Among Guizhou breeds, Baiyi black-bone and Guizhou yellow chicken displayed the lowest genetic diversity, as the 2 breeds exhibit lower PN and heterozygosity, the extent of linkage disequilibrium is higher. According to the LD pattern, Guizhou indigenous breeds can be divided into 3 categories. Population structure analysis showed a certain degree of genetic differentiation among local chickens in Guizhou. We argue that Chishui black-bone and Puan black-bone chickens are 2 different geographical regional groups of the same breed. In principal component analysis, individuals from the 2 groups clustered together, and the phylogenetic tree results showed that the 2 groups clustered together to form a branch independent of other breeds, and they displayed an identical pattern of ancestral lineage composition. The research results will provide a reference for protecting local chicken genetic resources in Guizhou Province and promote the protection and utilization of genetic resources.

Key words: Guizhou local chicken, SNP chip, genetic diversity, population structure, conservation

INTRODUCTION

Genetic diversity refers to the sum of all genetic information of all living things on Earth (Ellegren and Galtier, 2016). Generally speaking, the higher genetic diversity of a group represents its ability to adapt to the environment (DeWoody et al., 2021). We can understand the historical origin, evolutionary process, and germplasm characteristics of a breed through genetic diversity analysis (Liu et al., 2023; Wang et al., 2015; Zhang et al., 2020b), which is of great significance to breed improvement and protection (Gu et al., 2024; Wang et al., 2015). Chickens (Gallus gallus) are domestic animals widely raised around the world and play an essential role in food, sacrifices, entertainment, decoration, and scientific research, and are closely related to human life (Hata et al., 2021; Liu et al., 2006; Miao et al., 2013; Wang et al., 2020). The complex geographical environment, diverse climate, and culture of China have cultivated more than 110 local chicken breeds with distinctive characteristics (Ren et al., 2023). Guizhou Province has complex landforms and ecosystems, diverse resources, and culture (Li et al., 2014), these unique advantages are conducive to developing indigenous chickens. According to the latest official survey (China National Commission of Animal Genetics Resources, 2021), 8 local chicken breeds were originally distributed in Guizhou Province. Among these local chicken breeds, Puding gaojiao (GJ) and Yaoshan chickens (YS) are characterized by large size and good meat quality. Weining chickens (WN) have a strong ability to adapt to the cold environment and good reproductive performance. Xingyi aijiao chickens (XY) have compact bodies and short legs. Changshun green egg chickens (CS) are well known for high-quality green eggs. Qiandongnan xiaoxiang chickens (XX) exhibit desirable characteristics such as beautiful appearance, good foraging ability, and environmental adaptability. Wumeng black-bone chickens (WM) and Chishui black-bone chickens (CW) both have black feathers and high medicinal value. In addition, there are several uninvestigated native breeds in Guizhou Province. Guizhou yellow chicken (GH) with yellow feathers, beak, and shanks, is an indigenous chicken breed bred in Guizhou Province. Puan black-bone chickens (PA) and Qianhua black-bone chickens (QH) are characterized by large size, strong foraging ability, and tender meat. Baiyi black-bone chicken (BY) is a characteristic population with a long local breeding history with black feathers and white skin. Manyi black-bone chickens (MY) have black feathers and red cockscomb. Wumeng-crested chicken (WF) is a unique breed with a crested head and black bones. Huangping yellow chickens (JH), and Xianglu mountain chickens (XL) are characterized as strong and aggressive. Fanjing yu chickens (FJ) are famous for their white feet. These breeds are renowned for high medicinal value, good meat quality, excellent egg quality, and strong stress resistance (Liu et al., 2021; Mu et al., 2021; Xu et al., 2023), which plays an important role in the economic production and poultry improvement of family farms (Li et al., 2023; Mtileni et al., 2011). However, indigenous chicken breeds have slow growth, high feed-to-meat ratio, and low reproductive performance (Padhi, 2016). They also have a long growth cycle and poor economic benefits. To meet market demand, there has been rapid genetic breeding acceleration, and a large influx of foreign commercial chickens. This has led to the loss or alteration of certain genetic traits of indigenous chickens, including adaptability and disease resistance (Nie et al., 2019; Rubin et al., 2010). To protect these excellent breeding materials, it is particularly urgent to carry out an investigation and evaluation of genetic resources. Local breeds of Guizhou are an essential part of the local chicken resources of China. The protection and utilization of genetic resources are of great significance to the sustainable development of the poultry industry (Zhi et al., 2023).

Currently, research on the genetic diversity and genetic structure of indigenous chickens in Guizhou Province mainly used mitochondrial DNA (Liu et al., 2020a, 2020b), and SNP chip (Liu et al., 2021). However, previous studies either have limited coverage of varieties or exhibit certain methodological limitations. In recent years, gene chip typing technology has made genome-wide SNP analysis more accurate, faster, and cheaper. It has been widely used in breeding and genetic resource evaluation. Genome-wide SNP chip typing technology was widely used in the evaluation of genetic resources of Chinese gamecock gamecockss (Ren et al., 2023), chickens (Gao et al., 2023; Zhang et al., 2020a), pigs (Wang et al., 2021), cattle (Van Marle-Köster et al., 2021), sheep (Deniskova et al., 2018) and other species (Tang et al., 2023; Zhang et al., 2018a). The Affy 600 K SNP chip is widely used in chickens (Kranis et al., 2013). However, the chip is "biased," and the marking information mainly comes from Western commercial varieties. The Affy 55K genotyping array marking information comes from Chinese and foreign breeds, and the information source is more extensive (Liu et al., 2019). This array has broad application prospects in research areas such as evaluating indigenous chicken germplasm resources and genome selection. For instance, the Affy 55K genotyping array was used to conduct genetic analysis on Jiangxi indigenous chickens and identify candidate genes for black feathers (Mao et al., 2019). The researcher used fill-in sequencing data and chip data to predict the genome of 3 slaughter traits of white-feather broiler chickens based on the GBLUP method and compared the accuracy. The results show that the accuracy of genomic breeding value predictions with populated sequencing data is not significantly improved compared to the results from the Affy 55K genotyping array (Yin et al., 2023). In this study, we aimed to evaluate the genetic diversity and population structure of seventeen native chicken breeds using the Affy 55K genotyping array. This research provides scientific data and theoretical support for the information for the protection and utilization of indigenous chicken genetic resources.

MATERIALS AND METHODS

Samples Collection and Genotyping

We collected a total of 496 chicken blood samples from seventeen indigenous chicken populations distributed in Guizhou Province, namely 8 indigenous breeds Weining (WN, n = 27), Wumeng black-bone (WM, n = 30), Chishui black-bone (CW, n = 30), Changshun green egg (CS, n = 28), Qiandongnan xiaoxiang (XX, n = 29), Xingyi aijiao (XY, n = 29), Puding gaojiao (GJ, n = 30), and Yaoshan (YS, n = 30) chickens, 9 indigenous breed populations including Huangping yellow (JH, n = 30), Xianglu mountain (XL, n = 30), Qianhua black-bone (QH, n = 30), Wumeng-crested (WF, n = 30), Puan black-bone (PA, n = 29), Fanjing yu (FJ, n = 30), Manyi black-bone (MY, n = 25), Baiyi black-bone (BY, n = 30), and Guizhou yellow (GH, n = 29) chickens. Complex geographical environments and climatic factors resulted in the different phenotypes of these breeds (Figure 1). The samples mainly came from the core production areas and breeding farms of various chicken breeds, details are summarized in Table 1. Blood samples were collected according to local ethical standards. Approximately 1.0 mL of blood (EDTA anticoagulated) was collected from the wing vein of live chickens using a blood collection needle and stored at -20°C until use. Genomic DNA was extracted from a blood sample using the CWE9600 Magbead Blood DNA Kit (Jiangsu Cowin Biotech Co., Ltd.). Genomic DNA for all samples was quantified using agarose gel electrophoresis and the Nanodrop ND-200 spectrophotometer (Thermo Scientific). And gDNA concentrations for all samples reach 50 ng/uL. Genotyping was performed using an Affy 55K genotyping array (Beijing Compass Biotechnology Co., Ltd), including amplification, resuspended, hybridization, stained, and imaged on an Illumina iScan Reader. The 55K genotype data were then converted into PLINK v1.9 (Purcell et al., 2007) input files for data analysis.

Figure 1.

Figure 1

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Geographic distribution of 17 local chicken breeds in Guizhou Province, China. These chicken breeds exhibit distinct phenotypes. The blue fonts are the names of autonomous prefectures and cities in Guizhou. Weining chickens (WN), Wumeng black-bone chickens (WM), Chishui black-bone chickens (CW), Changshun green egg chickens (CS), Qiandongnan xiaoxiang chickens (XX), Xingyi aijiao chickens (XY), Puding gaojiao chickens (GJ), Yaoshan chickens (YS), Huangping yellow chickens (JH), Xianglu mountain chickens(XL), Qianhua black-bone chickens (QH), Wumeng-crested chickens (WF), Puan black-bone chickens (PA), Fanjing yu chickens (FJ), Manyi black-bone chickens (MY), Baiyi black-bone chickens (BY), Guizhou yellow chickens (GH).

Table 1.

Number of 17 chicken breeds and source of sample information.

Chicken breed Abb. Sample size Sampling location
Weining chicken WN 27 Nayong County, Guizhou province
Wumeng black-bone chicken WM 30 Nayong County, Guizhou Province
Chishui black-bone chicken CW 30 Nayong County, Guizhou Province
Changshun green egg chicken CS 28 Nayong County, Guizhou Province
Qiandongnan xiaoxiang chicken XX 29 Nayong County, Guizhou Province
Xingyi aijiao chicken XY 29 Nayong County, Guizhou Province
Puding gaojiao chicken GJ 30 Anshun City, Guizhou Province
Yaoshan chicken YS 30 Libo County, Guizhou Province
Huangping yellow chicken JH 30 Huangping County, Guizhou Province
Xianglu mountain chicken XL 30 Kaili City, Guizhou Province
Qianhua black-bone chicken QH 30 Dafang County, Guizhou Province
Wumeng-crested chicken WF 30 Liupanshui City, Guizhou Province
Puan black-bone chicken PA 29 Puan County, Guizhou Province
Fanjing yu chickens FJ 30 Tongren City, Guizhou province
Manyi black-bone chicken MY 25 Tongren City, Guizhou Province
Baiyi black-bone chicken BY 30 Guiyang City, Guizhou Province
Guizhou yellow chicken GH 29 Huaxi County, Guizhou Province
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Data Quality Control and Analysis

Plink (v1.90) software was used for data quality control (Purcell et al., 2007). The quality control standards were: using sites on autosomal chromosomes with SNP detection rate ≥90%, individual detection rate ≥90%, and MAF ≥0.01. Table 2 showed 55023 SNP marker typing results were detected; 3575 markers had MAF less than 0.01, and 1688 markers had SNP detection rates less than 0.90. There were 3077 markers on the Z chromosome, 26 on the W chromosome, and 8 inserted or deleted markers, resulting in 46,649 loci for subsequent analysis.

Table 2.

SNP quality control statistics.

Quality control standard Numbers of SNPs
(Total number of SNPs) 55,023
(SNP with MAF < 0.01) 3,575
<0.90 (SNP with callrate < 0.90) 1,688
(SNPs on chromosome Z) 3,077
(SNPs on chromosome W) 26
(insertion/deletion) 8
(SNPs used after quality control) 46,649
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Population Structure and Genetic Diversity

Plink (V1.90) software was used to calculate the effective population content (Ne), expected heterozygosity (He), observed heterozygosity (Ho), polymorphic marker ratio (PN), and Nucleotide diversity (Pi), and other parameters. Used GCTA (V1.94) to perform PCA (Principal Component Analysis) analysis (Yang et al., 2011) and used whole-genome markers to construct a genomic relationship G matrix (VanRaden 2008). Plink (V1.90) was used to construct a genome-wide identity by State (IBS) distance matrix, and based on this, an evolutionary tree was constructed through the Neighbor-Joining (NJ) method (Kumar et al., 2018). Use Admixture software to conduct population structure analysis and set a data set with parameter K=2∼19 (Alexander, et al., 2009). FST was used to measure the degree of differentiation between populations (Weir and Cockerham, 1984), and the value range of FST is 0∼1. When the value is 0, it means that the 2 populations are randomly mating and the genotypes are completely similar. If it is 1, it is completely different.

RESULTS

Analysis of Population Genetic Diversity

The genetic diversity index is shown in Table 3. Among the 17 breeds, except for the 2 groups of GJ and MY, the observed heterozygosity was slightly higher than the expected heterozygosity. BY had the lowest PN, Pi, Ho, and He, which were 0.7275, 0.3366, 0.3373, and 0.3307, respectively. WN had the highest Ho, He, and Pi, which were 0.3780, 0.3704, and 0.3776, respectively. The effective population content of XX was the highest (Ne=6). Linkage disequilibrium (LD) decay patterns can provide detailed information about the evolution of populations. Guizhou indigenous breeds could be divided into 3 categories according to the LD pattern (Figure 2): The first category was BY and GH, with higher attenuation coefficients, indicating that the 2 breeds are highly selected. The second category had XY, QH, CS, XL, and WF, which have relatively rich genetic diversity and may have undergone a certain degree of artificial selection. The third category included XX, WN, WM, MY, GJ, JH, PA, FJ, YS, and CW, with higher attenuation coefficients. This suggests that they have greater genetic diversity and are better protected.

Table 3.

Genetic diversity parameters of chicken from different breeds.

Breed Ne PN He Ho Pi
YS 5.8 0.8481 0.3583 0.3637 0.3644
CS 5.7 0.8094 0.3482 0.3591 0.3546
CW 5.8 0.8445 0.3626 0.3703 0.3689
XY 5.8 0.8001 0.3537 0.3579 0.3599
WM 5.8 0.8631 0.3678 0.3752 0.374
XX 6 0.8328 0.3513 0.3551 0.3572
GJ 4.6 0.8247 0.3520 0.3510 0.358
WN 4.6 0.8615 0.3704 0.3780 0.3776
BY 5.8 0.7275 0.3307 0.3373 0.3366
PA 5.8 0.8604 0.3676 0.3705 0.3741
QH 5.7 0.7975 0.3440 0.3547 0.3499
WF 5.8 0.8116 0.3455 0.3528 0.3514
JH 5.8 0.8539 0.3605 0.3641 0.3667
MY 4.4 0.8374 0.3581 0.3548 0.3655
XL 5.8 0.8098 0.3517 0.3558 0.3576
FJ 4.6 0.8563 0.3616 0.3673 0.368
GH 5.5 0.7692 0.3546 0.3589 0.3608
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Ne: effective population content; Ho: observed heterozygosity; He: expected heterozygosity; Pi: nucleotide diversity; PN: polymorphic marker ratio.

Figure 2.

Figure 2

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Linkage disequilibrium (LD) decay for the seventeen breeds. LD decay was determined by r2 against the distance between polymorphic sites.

Analysis of Population Genetic Structure

Principal component analysis (PCA), phylogenetic tree, and population structure analysis were used in this study to reveal the population structure of indigenous chicken breeds in Guizhou Province. The PCA results showed that the first 2 principal components account for 19.22% (PC1) and 15.67% (PC2) of the total variability (Figure 3). All groups of indigenous chicken breeds in Guizhou were divided into 7 clusters to reflect their different geographical origins. Among them, 4 independent populations were identified as GH, QH, BY, and XY. GJ and WF were grouped together, while WN, WM, PA, and CW were grouped into another category. Furthermore, a category was created by grouping MY, FJ, YS, XX, XL, CS, and JH. QH was distributed in independent clusters, but the gatherings were relatively scattered.

Figure 3.

Figure 3

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The PCA plot of chicken populations. PC1 and PC2 explained 19.22% and 15.66% of the observed variance, respectively.

The results of the phylogenetic tree analysis, as illustrated in Figure 4 that the 17 breeds can be divided into 8 clades. These clades were as follows: BY was grouped into 1 branch, while WF, QH, and GJ were grouped into another. XL, XX, and YS were grouped into 1 branch, while JH was in another. Similarly, MY and FJ were grouped into 1 branch. In contrast, CS formed an independent branch, and some MY chicken individuals were clustered into CS. CW and PA belonged to the same branch. Furthermore, indigenous chicken breeds, including WN, WM, GH, and XY, were grouped into another category. Except for CW and PA, the clustering situation of other chicken breeds was roughly consistent with the geographical distribution and PCA results.

Figure 4.

Figure 4

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Neighbor-joining tree constructed using MEGA.

The results of the ADMIXTURE analysis for the 17 local breeds with K values from 2 to 19 are shown in Supplementary Data 1, and the lowest cross-validation error was found at K=15 (Figure 5A). As shown in Figure 5B, at K = 2, GH was separated from the other breeds. The genetic backgrounds of GH and other breeds are significantly different. At K = 3, we found a strong genetic differentiation of the BY from all other studied breeds that persisted at higher K values. At K = 4 and K = 6, QH and XY were separated. The distinct genetic remoteness of the 4 breeds was consistent with the average pairwise FST values and the PCA finds. Notably, when K ranged from 2 to 5, GH and about half of XY individuals showed similar ancestral components, and were not completely separated until K = 6. From K = 9 to higher values, a high degree of genetic heterogeneity was observed for the FJ, which revealed mixed ancestry (Supplementary Data 1). At the best fit (K = 15), WN and WM, CW and PA were displayed as having similar ancestry components. It is worth noting that no matter what the value of K is, WN and WM always have similar ancestral structures. In addition, potential extensive genetic exchanges were clearly observed during the evolution of Guizhou local chicken populations.

Figure 5.

Figure 5

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Patterns of ancestral lineage composition in the 17 chicken breeds. The different numbers of assumed ancestors (from K = 2 ∼ 6) were assumed for these breeds (B). The optimal number of assumed ancestors was fifteen (K = 15), at which point the cross-validation error reached the lowest level (A).

The pairwise genetic differentiation index between various breeds was shown in Table 4. The FST value range was 0.04 (WN and WM) to 0.19 (GH and BY). BY showed a medium to high degree of differentiation from other breeds, with an average FST value of 0.15. FJ exhibited the lowest FST value compared with other indigenous breeds, with an average FST value of 0.8. The differentiation between WN and WM, CW and PA is minimal, with FST values of 0.04 and 0.05, respectively. GH was highly differentiated from other indigenous breeds, with FST between 0.13 and 0.19.

Table 4.

FST statistics between populations.

BY CS CW FJ GH GJ JH MY PA QH WF WM WN XL XX XY
CS 0.16
CW 0.15 0.11
FJ 0.13 0.09 0.08
GH 0.19 0.16 0.14 0.13
GJ 0.14 0.10 0.09 0.07 0.15
JH 0.14 0.09 0.08 0.06 0.14 0.08
MY 0.14 0.09 0.08 0.06 0.14 0.08 0.06
PA 0.14 0.09 0.05 0.06 0.13 0.08 0.07 0.07
QH 0.16 0.12 0.11 0.10 0.16 0.10 0.10 0.10 0.10
WF 0.15 0.11 0.10 0.09 0.16 0.09 0.09 0.09 0.09 0.11
WM 0.14 0.10 0.08 0.07 0.13 0.09 0.07 0.08 0.07 0.11 0.10
WN 0.14 0.09 0.08 0.06 0.13 0.08 0.07 0.07 0.06 0.10 0.09 0.04
XL 0.16 0.12 0.11 0.09 0.16 0.10 0.09 0.09 0.09 0.12 0.11 0.10 0.09
XX 0.15 0.10 0.10 0.07 0.15 0.08 0.08 0.07 0.08 0.11 0.09 0.09 0.08 0.09
XY 0.17 0.13 0.12 0.11 0.14 0.12 0.11 0.11 0.11 0.14 0.13 0.11 0.11 0.13 0.12
YS 0.14 0.10 0.09 0.07 0.14 0.08 0.07 0.07 0.07 0.11 0.09 0.08 0.07 0.09 0.07 0.11
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FST = 0–0.05 means very little differentiation, 0.05–0.15 means moderate differentiation, 0.15–0.25 means a high degree of differentiation, and FST > 0.25 means extreme differentiation.

Kinship Analysis

The genetic relationship statistics of each breed are shown in Table 5. The IBS genetic distance of each breed was 0.269 (BY) to 0.298 (WN). It confirmed a long genetic distance between individuals in different groups. The IBS genetic distance matrix showed that the genetic distance between most individuals of each breed was relatively far (Supplementary Data 2 and 3). Nevertheless, some individuals of FJ, GJ, and MY had close genetic distances and close genetic relationships and might have inbreeding risks (Figure 6). The genomic kinship coefficient was 0.000817 (XX) to 0.0244 (FJ), indicated that the genetic relationship between individuals in each group was distant. The G matrix visualization showed that some FJ, GJ, and BY chicken individuals were closely related (Figure 7). Consistent with the IBS matrix analysis results, it was found that the 3 varieties have an inbreeding trend, and relevant conservation measures need to be taken or strengthened.

Table 5.

Relationships between populations.

Breed Genomic kinship Genetic distance
BY 0.00518 ± 0.00046 0.269 ± 0.000309
CS 0.00602 ± 0.000669 0.28 ± 0.000178
CW 0.00145 ± 0.00024 0.291 ± 5.27e-05
FJ 0.0244 ± 0.00655 0.292 ± 0.000618
GH 0.0126 ± 0.00328 0.288 ± 0.00028
GJ 0.0232 ± 0.00412 0.287 ± 0.000429
JH 0.0084 ± 0.00129 0.292 ± 0.000177
MY 0.0146 ± 0.00358 0.294 ± 0.000471
PA 0.00228 ± 0.000277 0.297 ± 4.67e-05
QH 0.0166 ± 0.00247 0.277 ± 0.000344
WF 0.00793 ± 0.00109 0.279 ± 0.00017
WM 0.00634 ± 0.000741 0.295 ± 0.000144
WN 0.0104 ± 0.0031 0.298 ± 0.000228
XL 0.00356 ± 0.00075 0.285 ± 9.04e-05
XX 0.000817 ± 3.38e-05 0.285 ± 1.98e-05
XY 0.00484 ± 0.000845 0.287 ± 9.24e-05
YS 0.0053 ± 0.000875 0.289 ± 9.55e-05
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Figure 6.

Figure 6

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The visualization results of the IBS distance matrix of FJ (A), GJ (B), and MY (C). Each small square in the IBS distance matrix represents the value of genetic distance between 2 pairs from the first sample to the last sample, the larger the value, the closer it is to red, that is, the larger the genetic distance between 2 individuals, and vice versa.

Figure 7.

Figure 7

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The visualization results of the G matrix of FJ (A), GJ (B), and MY (C). In the G matrix results, each small square represents the value of the relationship between 2 pairs from the first sample to the last sample, the larger the value, the closer it is to red, that is, the closer relationship between 2 individuals.

DISCUSSION

This study used whole-genome SNP chips to analyze the genetic diversity and population structure of 17 indigenous chicken breeds in Guizhou Province. It analyzed the genetic diversity of indigenous breeds in Guizhou Province through parameters such as Ne, PN, He, Ho, and Pi. Pi refers to nucleotide diversity, and polymorphic marker ratio (PN) refers to the proportion of polymorphic sites in the target population to the total sites (Danecek et al., 2011). Generally, the larger the Pi and PN values, the greater the genetic diversity and the richer the sex (Li et al., 2020). Expected heterozygosity (He) refers to the probability of heterozygosity at any site in any individual in the population. Observed heterozygosity (Ho) refers to the proportion of heterozygous individuals at a specific locus in the population to the total number of individuals (Nei and Roychoudhury, 1974). The higher the Ho value represents the richer genetic diversity of the population (Sun et al., 2017). This study showed that the overall genetic diversity of indigenous chicken breeds in Guizhou was high, similar to previous research results (Xu et al., 2023). The genetic diversity of BY chicken was the lowest among all groups (PN = 0.7275, Pi = 0.3366, Ho = 0.3373, He = 0.3307); it might be due to the insufficient development and utilization of this breed, the low population size, and the increased degree of inbreeding, resulted in inbreeding depression and reduction in genetic diversity (Doekes, et al., 2021). The Ne value was estimated from the linkage disequilibrium level and was often used to evaluate the rate of population genetic drift (Wright, 1931). In this study, the Ne of MY was 4.4; it might be that the effective population content had been reduced due to strong selection in this population recently (Tolone et al., 2023). FJ, JH, and PA had richer genetic diversity among the indigenous breeds. The reason might be that these breeds had not undergone strict systematic breeding. However, some individuals within the breed were closely related, so corresponding conservation measures should be taken to control inbreeding or hybridization and protect these precious indigenous chicken breeds (Qanbari et al., 2019). LD analysis reflects the intensity of selection, breeding systems, and genetic diversity of different groups (Waples et al., 2016). The difference in each group's selection degree could be inferred through the LD decay rate. Generally, the slower the LD decay rate, the higher the degree of selection (Fu et al., 2015). According to the LD attenuation pattern, the indigenous breeds in this study could be divided into 3 categories: The first category was GH and BY. The slow decay rate indicated that the 2 groups were subject to high selection, consistent with the breeding history or current conservation status (Fu and Hua, 2000; Jian et al., 2001; Liu, 2023; Yu 1987). The second category was XY, QH, CS, XL, and WF. The third category was XX, WN, WM, PA, CW, GJ, JH, FJ, YS, and MY, with a lower attenuation coefficient and relatively rich genetic diversity. According to the LD analysis results, strengthening the breeding conservation measures of GH and BY was recommended. The genetic diversity of indigenous chicken breeds in Guizhou in this study was not entirely consistent with previous studies, which might be related to changes in conservation priorities and schemes (Gao et al., 2023; Zhang et al., 2018b).

PCA results confirmed that indigenous chicken breeds in Guizhou might have 7 geographical origins. For instance, GH, BY, QH, and XY were genetically far away from other chicken breeds, revealing relatively consistent geographical origins. The QH chicken individuals gathered together but were highly dispersed. It was speculated that hybridization might be an essential reason for their low genetic diversity. The phylogenetic tree results showed that indigenous chicken breeds in Guizhou Province could be divided into 8 clades, and the clustering results were roughly consistent with the PCA results and geographical distribution range. CW and PA chicken were grouped, indicating that the 2 species were closely related. However, the 2 breeds were located in the north and southwest of Guizhou Province. From the geographical point of view, the genetic relationship between the 2 breeds should be relatively distant. There may be gene flow between them, but the situation was similar between GH and XY. In the study of Ren et al. (2023), they suggested that gene flow was caused by consciously or unconsciously mixing within and between local chicken populations. We should prevent such incidents from happening again when we protect these chicken breeds in the future. There was a certain degree of mixing between WN and WM when clustered, the result was similar to the results of previous studies, and the result was similar to the results of previous studies (Liu et al., 2021; Xu et al., 2023). The reason may be that the 2 chicken species were distributed in the Wumeng Mountains of the Yunnan-Guizhou Plateau and belonged to the same 2 groups of Wumeng Chicken.

Admixture analysis showed that at K = 2, GH was separated from the other breeds. The genetic backgrounds of GH and other breeds are significantly different. The reason may be that the Plymouth Rock Buff and New Hampshire Chicken play an important role in the breeding process of Guizhou yellow chicken (Yu, 1987). At K = 3, we found a strong genetic differentiation of the BY from all other studied breeds that persisted at higher K-values. At K = 4 and K = 6, QH and XY were separated. The distinct genetic remoteness of the 4 breeds was consistent with the average pairwise FST values and the PCA finds. From K = 9 to higher values, a high degree of genetic heterogeneity was observed for the FJ, which revealed mixed ancestry. FJ was affected by the genetic mixture of other breeds, and its bloodline was relatively complex. This might be caused by FJ's extensive breeding and management, the indigenous farmers' weak awareness of protection, and random crossbreeding (Zhang et al., 2022). At the best fit (K = 15), WM and WN had more identical ancestral components, indicating that the 2 have similar genetic backgrounds, which might be related to their similar geographical distribution. CW and PA also showed similar genetic backgrounds, Wu et al. (2018) reported that the genetic distance between Guizhou black-bone chicken populations was relatively close. According to current relevant records, it could be speculated that CW played an important role in the breeding process of PA. It is worth noting that no matter what the value of K is, WN and WM always have similar ancestral structures. Judging from Admixture's genetic mixing ratio, BY, GH, and XL had a single pure ancestor. In addition, potential extensive genetic exchanges were clearly observed during the evolution of Guizhou local chicken populations. The phylogenetic tree showed that FJ and MY had the closest genetic relationship. Combined with the Admixture results, it could be inferred that there was genetic mixing between the 2 breeds. Due to the 2 breeds' close geographic distribution range, genetic mixing occurs due to human activities, and further purification of FJ and MY was required.

The above analysis showed a certain degree of genetic differentiation among indigenous chicken breeds in Guizhou Province. Among them, the degree of differentiation between QH, GH, BY, XY, and other native breeds is relatively high. The genetic differentiation index between populations was used to measure the degree of differentiation of the population (Meirmans and Hedrick, 2011), with a value ranging from 0 to 1. The degree of genetic differentiation was divided into 4 levels according to the FST value (Hartl et al., 1997): FST =0∼0.05 means very little differentiation, 0.05 to 0.15 means moderate differentiation, 0.15 to 0.25 means a high degree of differentiation, and FST > 0.25 means extreme differentiation. In this study, the differentiation index of each group ranged from 0.04 to 0.19, among which the degree of differentiation between WN and WM (0.04), CW, and PA chicken (0.05) were minimal, and the remaining breeds showed a medium to high degree of differentiation. QH, GH, BY, XY, and other indigenous breeds had a higher degree of differentiation, with average FST values of 0.116, 0.147, 0.150, and 0.123, respectively. In the study of Wu et al. (2023), they indicated that human management factors played a greater role in the genetic differentiation of the Dutch traditional chicken breeds. Combined with the actual production situation in Guizhou Province, artificial isolation may play an equally important role in the emergence of moderate to high genetic differentiation in local chicken populations. The BY and GH populations are geographically separated by 70 km, but their genetic differentiation index is the highest, which is caused by human intervention for different production purposes. The FST value (0.13) between WN and GH indicated that there was moderate genetic differentiation between them, which may be due to the long-term closed breeding of GH.

GH was a dual-purpose breed bred by the former Guizhou Agricultural College in the 1980s through the crossbreeding of 3 breeds, and its comprehensive performance was superior to that of other indigenous chicken breeds in Guizhou Province. Since its breeding, it has been widely promoted in Guizhou Province and surrounding areas (Yang et al., 2022), which may particularly impact indigenous chicken breeds in Guizhou. Admixture results indicated XY was mixed with a small amount of GH. This result confirmed the speculation that GH was used for hybrid improvement during the promotion process. The QH was mainly distributed in Xinren Township, Qianxi County, and was an excellent indigenous resource in Guizhou Province. However, the relatively backward production model and weak awareness of protection and development had caused the QH to be invaded by exotic chicken breeds, and its germplasm resources were threatened. PCA and phylogenetic analysis results confirmed that BY was most obviously differentiated from other breeds. The central production area of BY chicken was located in Baiyi Town, Guiyang City. The area had undulating terrain and inconvenient transportation. After long-term selection and breeding, a breed with a significant genetic distance from other indigenous breeds had been formed. We consider that strong artificial selection and distance isolation are the main driving forces of genetic differentiation (Luo et al., 2020).

Identification of genetic relationships could formulate reasonable strategies for the conservation and utilization process in indigenous chickens. Identical by state (IBS) refers to the probability that the observed values of 2 individuals at the same locus were the same. IBS only considered the similarity of genetic markers or alleles between individuals and could analyze the genetic relationship of the group. The G matrix could more truly reflect the genetic relationship between individuals. The analysis showed that the genetic distance between different individuals of various indigenous chicken breeds in Guizhou Province was far away, and the genetic relationship was far away in this study. A few individuals had close genetic distance and close genetic relationships. Some FJ, GJ, and MY individuals were closely related, and the group might have a certain degree of inbreeding. The reason might be due to changes in the population's genetic structure caused by closed breeding or a small population size. Breeding conservation measures need to be strengthened to avoid inbreeding depression.

CONCLUSION

In summary, our results suggest that the genetic diversity of native chicken breeds in Guizhou Province was relatively rich, among which BY and GH had the lowest genetic diversity, and there is a certain genetic differentiation between different groups. FJ chicken could be facing a high risk of admixture from other breeds. According to the population structure and genetic distance analysis results, we argue that CW and PA belong to different groups of the same breed. Our results will help to better understand the genetic diversity and population structure of Guizhou local breeds and lay the foundation for the protection, production, applications, and scientific search.

DISCLOSURES

The authors declare that they have no competing interests.

ACKNOWLEDGMENTS

This work was supported by the Guizhou Provincial Science and Technology Project (QKH-ZC2022-key34) and the Natural Science Research Project of the Guizhou Provincial Department of Education (QJJ-ZK2022-061).

Author contributions: Fuping Zhang designed the experiments and revised the manuscript. Zhong Wang, and Hui Li designed the experiments. Sheng Wu performed the experiments and wrote and revised the manuscript. Lujiang Qu revised the manuscript. Zhiwen Chen and Xiaohong Zhou performed the experiments, analyzed the data, and wrote the manuscript. Yingping Tian, Yaozhou Jiang, and Qinsong Liu assisted in collecting samples. All authors read and approved the final manuscript.

Ethics statement: All animal works were conducted according to the guidelines for the care and use of experimental animals established by the Ministry of Agriculture and Rural Affairs of China. The Animal Care and Use Committee at Guizhou University specially approved this project (No.EAE-GZU-2024-E003).

Footnotes

Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2024.104383.

Appendix. Supplementary materials

Supplementary Data 1. The admixture plot for seventeen breeds was analyzed based on varying numbers of assumed ancestors (K = 2∼19).

mmc1.pdf (610KB, pdf)

Supplementary Data 2. The visualization results of the IBS distance matrix of seventeen local chicken breeds.

mmc2.pdf (1.2MB, pdf)

Supplementary Data 3. The visualization results of the G matrix of seventeen local chicken breeds.

mmc3.pdf (954.2KB, pdf)

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Associated Data

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Supplementary Materials

Supplementary Data 1. The admixture plot for seventeen breeds was analyzed based on varying numbers of assumed ancestors (K = 2∼19).

mmc1.pdf (610KB, pdf)

Supplementary Data 2. The visualization results of the IBS distance matrix of seventeen local chicken breeds.

mmc2.pdf (1.2MB, pdf)

Supplementary Data 3. The visualization results of the G matrix of seventeen local chicken breeds.

mmc3.pdf (954.2KB, pdf)

Articles from Poultry Science are provided here courtesy of Elsevier

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