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Article

Thai Local Chicken Breeds, Chee Fah and Fah Luang, Originated from Chinese Black-Boned Chicken with Introgression of Red Junglefowl and Domestic Chicken Breeds

by
Trifan Budi
1,2,†,
Worapong Singchat
1,3,†,
Nivit Tanglertpaibul
1,2,†,
Wongsathit Wongloet
1,3,
Aingorn Chaiyes
4,
Nattakan Ariyaraphong
1,3,5,
Worawit Thienpreecha
1,
Wannapa Wannakan
1,
Autchariyapron Mungmee
1,
Thanyapat Thong
1,
Pish Wattanadilokchatkun
1,
Thitipong Panthum
1,2,
Syed Farhan Ahmad
1,2,
Artem Lisachov
1,
Narongrit Muangmai
1,6,
Rattanaphon Chuenka
7,
Pollavat Prapattong
8,
Mitsuo Nunome
9,
Wiyada Chamchumroon
10,
Kyudong Han
1,11,12,
Santi Pornpipatsiri
13,
Thepchai Supnithi
14,
Min-Sheng Peng
15,16,
Jian-Lin Han
17,
Yoichi Matsuda
1,
Prateep Duengkae
1,3,
Phuechphol Noinafai
13 and
Kornsorn Srikulnath
1,2,3,5,18,19,*add Show full author list remove Hide full author list
1
Animal Genomics and Bioresource Research Unit (AGB Research Unit), Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand
2
Interdisciplinary Graduate Program in Bioscience, Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand
3
Special Research Unit for Wildlife Genomics (SRUWG), Department of Forest Biology, Faculty of Forestry, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand
4
School of Agriculture and Cooperatives, Sukhothai Thammathirat Open University, Pakkret Nonthaburi 11120, Thailand
5
Laboratory of Animal Cytogenetics and Comparative Genomics (ACCG), Department of Genetics, Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand
6
Department of Fishery Biology, Faculty of Fisheries, Kasetsart University, Bangkok 10900, Thailand
7
Faculty of Humanities, Kasetsart University, Bangkok 10900, Thailand
8
Mekong Sub-Region Arts and Culture Research Unit (MAC-MFU), Mae Fah Luang University, Chiang Rai 57100, Thailand
9
Department of Zoology, Faculty of Science, Okayama University of Science, Ridai-cho 1-1, Kita-ku, Okayama 700-0005, Japan
10
Deparment of National Park, Wildlife and Plant Conservation, Ministry of Natural Resources and Environment, Bangkok 10900, Thailand
11
Department of Microbiology, Dankook University, Cheonan 31116, Republic of Korea
12
Bio-Medical Engineering Core Facility Research Center, Dankook University, Cheonan 31116, Republic of Korea
13
Chiang Rai Provincial Livestock Office, Department of Livestock Development, Ministry of Agriculture and Cooperatives, Chiang Rai 57000, Thailand
14
National Electronics and Computer Technology Center (NECTEC), Khlong Luang 12120, Thailand
15
State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China
16
University of Chinese Academy of Sciences, Beijing 100049, China
17
CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100081, China
18
Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Bangkok 10900, Thailand
19
Center for Advanced Studies in Tropical Natural Resources, National Research University-Kasetsart University, Kasetsart University, Bangkok 10900, Thailand
 
add Show full affiliation list
 
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*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Sustainability 2023, 15(8), 6878; https://doi.org/10.3390/su15086878
Submission received: 25 February 2023 / Revised: 2 April 2023 / Accepted: 17 April 2023 / Published: 19 April 2023
(This article belongs to the Special Issue Biodiversity in Different Regions: Exploring Global Ecology Sustainability)
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Abstract

:
Knowledge of the genetic characteristics, origin, and local adaptation of chickens is essential to identify the traits required for chicken breeding programs. Chee Fah and Fah Luang are black-boned chicken breeds reared in Chiang Rai, Thailand. Chickens are an important part of the local economy and socio-culture; however, the genetic diversity, characteristics, and origins of these two breeds have been poorly studied. Here, we investigated the genetic diversity, gene pool, and origin of the Chee Fah and Fah Luang chickens using mitochondrial DNA D-loop (mtDNA D-loop) sequencing and microsatellite genotyping, as well as habitat suitability analysis using maximum entropy modeling. The MtDNA D-loop sequencing and microsatellite genotype analyses indicated that the Chee Fah and Fah Luang chickens shared haplogroups A, B, and CD with Chinese black-boned chickens. Gene pool analysis revealed that the Chee Fah and Fah Luang chickens have distinct genetic patterns compared to Thai domestic chickens and red junglefowl. Some gene pools of red junglefowl and other Thai domestic chickens were observed within the Chee Fah and Fah Luang chicken gene pool structures, suggesting genetic exchange. The data indicate that the Chee Fah and Fah Luang chickens originated from Chinese indigenous black-boned chicken breeds and experienced crossbreeding/hybridization and introgression with red junglefowl and other domestic breeds during domestication. Interestingly, the Chee Fah and Fah Luang chickens from Chiang Rai shared the same allelic gene pool, which was not shared with the Chee Fah and Fah Luang chickens from Mae Hong Son, suggesting at least two gene pool origins in the Chee Fah and Fah Luang chicken populations. Alternatively, different gene pools in the Chee Fah and Fah Luang chickens from different localities might be caused by differences in environmental factors, especially elevation.

1. Introduction

A decline in genetic resources has been globally observed as a consequence of the massive replacement of low-productive indigenous and local chicken breeds with highly productive commercial breeds (e.g., White Leghorns, brown egg layer, and commercial broilers) during the last century. New domestic chicken breeds, such as Ta Pao Thong and Nin Kaset, have been bred in Thailand over the last 20 years, with some being of critical concern, such as broilers and layers [1]. This genetic upgrading may have resulted in the loss of various genetic alleles that are adapted to the local tropical environment [2,3]. Climate change has increased environmental stresses that limit the survivability and sustainability of red junglefowl and domestic chickens worldwide [4,5]. Heat waves, acute heat stress, and fluctuating temperatures have caused considerable mortality in certain broiler and layer chicken breeds [6,7,8], whereas the production of indigenous and local chicken breeds is relatively stable under high temperature and humidity [9]. This leads us to predict that indigenous and local chicken breeds in tropical areas can survive in harsh environments because of their physiological and genetic adaptations [10,11,12]. The characterization and conservation of indigenous and local chicken breeds are thus necessary to preserve their genetic diversity and to conserve the traits of adaptability required in future environmental and production scenarios. These breeds are considered better components for crossbreeding to generate more resilient commercial lines [12,13,14].
The Chee Fah and Fah Luang Northern Thai domestic chicken breeds were discovered in Chiang Rai province (19°18′2.40″ N, 97°58′7.19″ E) [15]. They can be easily distinguished by black-dominated feathers, and most have black-colored earlobes and combs. They are also known as black-boned chickens [16]. These breeds are an integral part of the sociocultural and rural life of northern Thai local communities and an economical food source because black-boned chickens contain low fat and cholesterol, high protein and collagen, and high contents of carnosine and anserine compared to commercial breeds, which are advantageous for human health [16,17,18]. The Chee Fah and Fah Luang chickens were originally derived from Chinese indigenous black-boned chickens introduced by military refugees from the ex-Kuomintang army and/or the Yunnanese-Chinese before the 1950s [19]. Chiang Rai has a well-known Yunnanese-Chinese ethnic group. Chee Fah chickens weigh 891–1714 g at 16 weeks and produce between 43 and 124 eggs annually, whereas Fah Luang chickens weigh 917–1311 g at 16 weeks and produce up to 141 eggs per year. The market prices of the eggs and meat of these chicken breeds are relatively higher than those of commercial breeds [18], while the costs of Chee Fah and Fah Luang chickens and their products are lower than those of commercial varieties in remote highlands, such as in Chiang Rai, and fills a specific niche for the local people [20]. The Chee Fah and Fah Luang chickens have adapted to the low-temperature highland environment in Northern Thailand, whereas broiler and layer chickens struggle to grow under the same conditions [21]. In 2005, the Department of Livestock Development (Ministry of Agriculture and Cooperatives) registered the Chee Fah and Fah Luang as native local chicken breeds [22,23]. The Thai Government uses these breeds to promote food security for hill tribe communities and remote schools [24]. Despite their importance, the origin and breeding process of these breeds remain unclear. It is possible that the Chee Fah and Fah Luang chicken breeds were established by human populations that moved outward from ancestral territories in China and settled in new colonies in Chiang Rai. The origin of the Chee Fah and Fah Luang chicken breeds can be traced by investigating their genetic lineages and comparing their mitochondrial DNA haplotypes and genetic diversity with Thai and black-boned chicken breeds from China. Three hypotheses regarding their origins were tested. The genetic diversity of outward populations (the Chee Fah and Fah Luang chickens) can be explained by their geographic distance from founder populations as a measure of neutral genetic diversity resulting from genetic drift. The mitochondrial DNA D-loop (mtDNA D-loop) sequences of Chee Fah and Fah Luang chickens should be present in the same haplogroup or even haplotype as Chinese indigenous black-boned chicken breeds (i). One expectation is the increase in genetic distances (increased differentiation) of the outward populations from the original ancestor/founder population [25]. Thus, the genetic distances of the mtDNA D-loop between Chee Fah and Fah Luang chickens and other Chinese indigenous black-boned chicken breeds may be higher than those of the Chinese indigenous black-boned chicken (ii).
There has been a long history of chicken domestication in Thailand [26,27]. One of the primary activities of the Animal Genomics and Bioresource Research Unit (AGB Research Unit), Faculty of Science, Kasetsart University, Thailand, is the preservation and characterization of domestic animals. We established “The Siam Chicken Bioresource Project” [28,29] to build a DNA fingerprint based on the microsatellite genotyping of red junglefowl and Thai domestic chicken breeds as a reference baseline for environmental habitat suitability. Chee Fah and Fah Luang chickens are thought to have experienced genetic introgression from red junglefowl and/or Thai domestic chicken breeds by crossbreeding and thereafter adapted to the Northern Thailand environment. In this scenario, the Chee Fah and Fah Luang chicken breeds might contain the genetic footprint of red junglefowl and/or other Thai domestic chicken breeds (iii). Investigations into the genetic variability of Chee Fah and Fah Luang chickens are needed to identify their genetic fingerprints and footprints. This study examined the genetic diversity of Chee Fah and Fah Luang chickens by screening the gene pool of each population from different localities. The genetic stocks of the two breeds were investigated using 28 microsatellite markers and mtDNA D-loop sequences. The results were compared with the large gene pool library under The Siam Chicken Bioresource Project. The spatial suitability of the Chee Fah and Fah Luang chickens was also evaluated using maximum entropy (MaxEnt) modeling [30] to precisely determine the optimal land suitability areas. Our results provide useful information regarding small chicken populations that have been managed to conserve their genetic variation in gene stocks, and to elucidate the future effectiveness of regional breeding programs.

2. Materials and Methods

2.1. Study Area, Environmental Data, and Spatial Habitat Suitability Model

Chiang Rai is Thailand’s northernmost province and forms part of the Golden Triangle region bordering Laos and Myanmar (19°00′20°30′ N, 99°15′100°45′ E). Environmental data collections, including elevation, distance to a river, vegetation index, tree canopy cover, and forest canopy height, and a spatial habitat suitability model were carried out as previously described by Singchat et al. [29] (see Supplementary Data S1).

2.2. Specimen Collection and DNA Extraction

Chee Fah and Fah Luang chickens were sampled at the Chiang Rai Livestock Research and Breeding Center (CRRBC), Chiang Rai (19°52′24.05″ N, 100°26′22.6″ E) and the Mae Hong Son Livestock Research and Breeding Center (MLRBC), Mae Hong Son (19°17′14″ N, 97°57′46″ E), Thailand. Detailed information on the sampled individuals is presented in Figure S1 and Table S1. No differences were found in the body weight, body size indicators, or feed consumption of the two breeds between CRRBC and MLRBC (Phuechphol Noinafai, personal communication). Blood specimens were collected from the brachial wing vein, followed by genomic DNA extraction using the standard salting-out protocol described by Supikamolseni et al. [31]. DNA quality and quantity were assessed using 1% agarose gel electrophoresis and a NanoDrop 2000 Spectrophotometer (Thermo Fisher Scientific, Wilmington, DE, USA). Experimental procedural approval for this study was granted by the Kasetsart University Animal Experiment Committee (Approval No: ACKU63-SCI-021 and ACKU63-SCI-022), and it was conducted in accordance with the Regulations on Animal Experiments at Kasetsart University.

2.3. Mitochondrial DNA D-Loop Sequencing, Quality Control, and Data Analysis

Mitochondrial DNA D-loop (mtDNA D-loop) fragments were amplified using the primer pair Gg_D-loop_1F (5′-AGGACTACGGCTTGAAAAGC-3′) and Gg_D-loop_4R (5′-CGCAACGCAGGTGTAGTC-3′) [32]. PCR amplification, sequence quality control, and mtDNA D-loop analysis were performed as previously described by Hata et al. [28] and Singchat et al. [29] (Supplementary Data S1). The mtDNA haplogroup nomenclature referred to Miao et al. [33]. All sequences were deposited in the DNA Data Bank of Japan (DDBJ) (https://www.ddbj.nig.ac.jp/, accessed on 25 November 2022) (accession numbers: LC740526–LC740564) (Table S1).

2.4. Microsatellite Genotyping and Data Analysis

Twenty-eight microsatellite primer sets were selected based on the recommendations of the Food and Agriculture Organization for chicken biodiversity assessments (Table S2). The 5-end of the forward primer of each primer set was labeled with a fluorescent dye (6-FAM or HEX; Macrogen Inc., Seoul, Republic of Korea). PCR amplification for microsatellite genotyping and analysis of genetic diversity and population structure based on microsatellite data, including allelic richness (AR), number of alleles per population (Na), polymorphic information content (PIC), heterozygosity (Ho and He), F-statistics (FIS and FST), and relatedness (r) were performed as described by Hata et al. [28] and Singchat et al. [29] (Supplementary Data S1). The genotypic data generated in this study were deposited in the Dryad Digital Repository Dataset (https://doi.org/10.5061/dryad.hhmgqnkm0, accessed on 15 January 2023).

3. Results

3.1. Land Suitability Map of Chee Fah and Fah Luang Chickens

Chiang Rai covers an area of 11,460 km2, and land unsuitable (p < 0.2) for the habitat of red junglefowl and domestic chickens was estimated at 9470 km2 (82.64% of the total area). The land area with very high suitability (p > 0.8) was predicted to be 5 km2 (0.04% of the total area), that with high suitability (0.6 < p ≤ 0.8) to be 158 km2 (1.38%), moderate suitability (0.4 < p ≤ 0.6) to be 794 km2 (6.93%), and least suitability (0.2 ≥ p ≤ 0.4) to be 1033 km2 (9.01%) (Figures S2–S5). The marginal response curves illustrate the influence of environmental variations on the occurrence probabilities of Chee Fah and Fah Luang chickens. The optimal environmental conditions for the occurrence probabilities of Chee Fah and Fah Luang chickens (MaxEnt model response curves) in the study area are presented in Figure S6. The optimal environment included tree canopy cover (0%), elevation (1200–1300 m), forest canopy height (1–13 m; shrub-tree), distance to the main river (10–1000 m), and NDVI (0.17–0.23; shrub and grassland).

3.2. Model Performance and Variable Importance of Habitat Suitability

An AUC value of 0.91 was obtained, indicating that the MaxEnt model was effective in predicting the potential distribution of the Chee Fah and Fah Luang chickens. The Jackknife method was used in the MaxEnt model, with results showing the weighted impact of different environmental factors on land suitability for the Chee Fah and Fah Luang chickens (Figure S7). The environmental factors affecting the potential distribution of the Chee Fah and Fah Luang chickens were elevation, NDVI, forest canopy height, tree canopy cover, and distance to the river, with contribution rates of 43.4%, 31.0%, 11.7%, 10.7%, and 3.2%, respectively. Elevation had the highest contribution rate, making it the most important factor affecting the potential distribution of local chickens (Figure S6).

3.3. Comparison of Environmental Factors between Local Chicken Farms in Mae Hong Son and Chiang Rai Provinces

Samples from Chiang Rai and Mae Hong Son provinces were collected from the Research and Breeding Center of the Department of Livestock. Environmental factors that might affect Chee Fah and Fah Luang chickens were compared between the two localities. A t-test showed statistically significant differences between the environmental variables of the local chicken farms (Figure S8 and Table S3).

3.4. Genetic Variability of Chee Fah and Fah Luang Chicken Populations Based on Mitochondrial DNA D-Loop Haplotypes

The mtDNA D-loop sequences of 18 haplotypes discovered in the two populations of Chee Fah and Fah Luang chickens had amplicons and alignment lengths of 1200 bp and 1001 bp, respectively. The haplotype diversity (h) and nucleotide diversity (π) of the overall mtDNA D-loop sequences were 0.994 ± 0.019 and 0.007 ± 0.00083, respectively (Table 1). The most common haplotype was CF5 (haplogroup B) in the Chee Fah chickens and FL4 (haplogroup B) in the Fah Luang chickens. All other haplotypes identified in the Chee Fah chickens were haplogroup B, whereas the haplotypes in the Fah Luang chickens were classified as haplogroups A, B, and CD (Figure 1 and Figure S9). To investigate the genetic differentiation between the two populations, we calculated the genetic differentiation coefficients within each population. The values ranged from 0.014 to 0.044 for FST and from 0.008 to 0.023 for GST. The ΦST values ranged from 0.014 to 0.044, and the average number of nucleotide substitutions per site between populations (Dxy) ranged from 0.006 to 0.007, while the net nucleotide substitutions per site between populations (Da) ranged from 0.0003 to 0.0008 (Table S4).
Phylogenetic analysis revealed that the Chee Fah and Fah Luang chickens were grouped into a clade with Chinese black-boned chickens (Dehua black, Guangxi black-boned, Zhuxiang, Huangyu black-boned, Jiangshan black-boned, Lueyang, Wuliangshan black-boned, Jinhu black-boned, Xichuan black-boned, Xuefang black-boned, Yanjin black-boned, Yugan black-boned breeds, and Silkies) and several Thai domestic breeds (Lueng Hang Khao, Pradu Hang Dam, Khaew Paree, and Fighting chickens) (Supplementary Figure S9). The mean pairwise distance shows that the Chee Fah and Fah Luang chickens had lower distances than Chinese black-boned chickens (1.41% and 1.51%, respectively), Thai domestic chickens (1.52% and 1.58%, respectively), and red junglefowl (2.26% (min, 0.79%; max, 3.39%) and 2.30% (min, 1.09%; max. 3.51%), respectively).

3.5. Genetic Variability of Chee Fah and Fah Luang Chicken Populations Based on Microsatellite Data

A total of 151 alleles were observed in the two populations of Chee Fah chickens, with a mean number of alleles per locus of 4.571 ± 0.233, whereas 213 alleles were observed in the Fah Luang chickens, with a mean number of alleles per locus of 4.982 ± 0.226 (Table 2). All allelic frequencies showed a significant departure from the Hardy–Weinberg equilibrium of the population, with multiple lines of evidence for linkage disequilibrium (Tables S5–S8). Null alleles were frequently found for LEI0094 and MCW0216 loci; however, all the markers listed were similarly treated. All populations of the Fah Luang chickens exhibited negative F values, while one population of the Chee Fah chickens, from CRRBC, showed a positive value (Table 2). The PIC of all populations of the Chee Fah and the Fah Luang chickens ranged from 0.00 to 0.893, while Shannon’s Information Index (I) was between 0.00 and 2.056 (Table S9). The mean Ho and He values were 0.562 ± 0.046 and 0.614 ± 0.023, respectively, for the Chee Fah chickens (Table 2 and Table S9). The mean Ho and He values were 0.558 ± 0.040 and 0.643 ± 0.022 for the Fah Luang chickens, respectively. All pairwise Ho and He values between the two populations of the Chee Fah and Fah Luang chickens were significantly different (Tables S10 and S11). The mean AR value of the Chee Fah chickens was 4.450 ± 1.650, and that of the Fah Luang chickens was 4.734 ± 1.564. The standard genetic diversity indices are summarized in Table 2 and Table S9.
Individual pairwise relatedness (r value) and inbreeding coefficient (FIS) were calculated to assess the probability of relatedness and inbreeding within the populations of the Chee Fah and Fah Luang chickens (Table S12). The mean pairwise r values in the Chee Fah and Fah Luang chickens were −0.031 ± 0.078 and −0.034 ± 0.067, respectively, whereas the FIS values were 0.093 ± 0.059 and 0.131 ± 0.054, respectively (Tables S13–S15). Analysis of molecular variance (AMOVA) showed that genetic variation accounted for 66% of the total variance within the populations and 34% between the populations of the Chee Fah chickens, and for 16% within the populations and 20% between the populations of the Fah Luang chickens (Table S16). Nei’s genetic distance values were 0.882 between the two populations of the Chee Fah chickens and 0.934 between the two populations of the Fah Luang chickens. The results of the principal coordinate analysis (PCoA) and discriminant analysis of principal components (DAPC) showed that the populations of each breed were classified into two clusters (Figure S10). This result is consistent with that of the model-based Bayesian clustering algorithms implemented in STRUCTURE, which generated two different population structure patterns with a low K-value (K = 2) (Figure S11). However, multiple clusters of the gene pool were observed in the CRRBC population with higher K-values, which were fitted with the highest posterior probability of ΔK and ln P(K) (Figures S11 and S12). Genetic selective sweep analysis revealed neutral or balanced selection for all populations, which was reflected by a relatively low FIS coupled with high He (Figure S13).

3.6. Genetic Differences among Chee Fah Chickens, Fah Luang Chickens, Red Junglefowl, and Other Thai Domestic Chicken Breeds

Multiple population clusters were observed based on PCoA and DAPC results (Figure 2 and Figure S14). The major gene pool clusters were derived from the red junglefowl. The Chee Fah and Fah Luang chickens tended to have different gene pools from the red junglefowl and domestic chicken clusters. In this analysis, we also included the comparison data of gene pool patterns between the Chee Fah and Fah Luang chickens and the reference baseline data from our previous studies, including red junglefowl and domestic chicken breeds [28,29]. STRUCTURE analysis revealed the highest posterior probability with one peak (K = 7), based on Evanno’s ΔK, whereas the mean ln P(K) showed a different peak (K = 20) (Figure 3 and Figure S15). Red junglefowl showed a variety of gene pool patterns, whereas the Chee Fah and Fah Luang chickens tended to show unique genetic patterns. The gene pool patterns of most Thai indigenous chicken breeds (Lueng Hang Khao, Chee, and Keaw Paree) were similar, except for Fighting chickens. A part of the gene pool of red junglefowl from Phetchaburi, Chiang Rai, and Khao Kho populations, as well as domestic chickens (Dong Tao, Mae Hong Son, and Fighting chickens), were observed in the Chee Fah and Fah Luang chicken gene pools at K = 25. By contrast, some parts of the Chee Fah and Fah Luang gene pools, which were derived from MLRBC, were observed in the Mae Hong Son chicken gene pool. No sign of a selective sweep was found in the gene pools of the Chee Fah and Fah Luang chickens or other Thai domestic chickens (Figure S16).

4. Discussion

4.1. Lineage of Chee Fah and Fah Luang Chickens Is the Same as Chinese Black-Boned Chicken Breeds

The Chee Fah and Fah Luang chickens are hypothesized to have originated from Chinese black-boned chicken breeds because the same types of breeds are bred in local sociocultural Chinese communities in Chiang Rai. Human migration from China to Thailand has enabled the introduction of Chinese black-boned chickens and other domestic animals alongside their human domesticators to Thailand [34,35,36]. MtDNA D-loop sequence variation has been extensively used to gain a better understanding of the genetic structures of chicken populations, their genetic characteristics, evolutionary relationships, and domestication history. MtDNA D-loop sequences of chickens have been classified into eight highly divergent maternal haplogroups (A–G and V) and six rare haplogroups (H–I and W–Z) [33,37]. The major haplogroups A and B are widely distributed in Asian regions (East and Southeast Asia), whereas haplogroup C is widely spread over East Asia (Japan and China). Haplogroup D is mostly found in Southeast Asian and Pacific (Fiji and Melanesia) populations, whereas haplotype F is restricted to Yunnan province of China, Thailand, and Myanmar [28,29,33,37]. Most Chinese black-boned chicken breeds contain haplogroups A, B, CD, and E [37]. The mtDNA D-loop sequences of the Chee Fah chickens were classified into haplogroup B, while the Fah Luang chickens had haplogroups A, B, and CD. This suggests that they originated from Chinese black-boned chickens and had a potential sociocultural role, such as traditional offerings to spirits in Chinese communities across Chiang Rai [38,39].
Black-boned chickens in China are renowned for their characteristic traits, such as black skin, bones, and muscles [40]. To identify the specific original Chinese black-boned chickens that were involved in the development of Chee Fah or Fah Luang chickens, mtDNA D-loop phylogenetic analysis was conducted to estimate the genetic distances among the red junglefowl, Thai domestic, and Chinese black-boned chicken breeds. The Chee Fah and Fah Luang chickens were solely positioned within a cluster of Chinese black-boned chicken breeds, but did not fall into any other lineages. This result is consistent with the complex breeding histories of Chinese black-boned chicken breeds, where the mtDNA D-loop sequence data may not discriminate them from other lineages [40]. Larger genetic distances were observed between the Chee Fah and Fah Luang chickens and Chinese black-boned chicken breeds than among the Chinese black-boned chicken breeds, but they were smaller than between red junglefowl or other Thai domestic chicken breeds and Chinese black-boned chicken breeds. These results suggest that genetic differentiation increases with geographic distance between populations or the movement distance of individuals away from their founders [25]. Genetic exchange (mating opportunities) between individuals is likely limited by geographic distance [25]. Many Chinese native breeds are characterized by slow growth, late maturity, and low production performance. This was also observed in the Chee Fah and Fah Luang chickens [17]. Studies of the genetic and physiological properties, such as melanin pigmentation and fibromelanosis [41,42], in the Chee Fah and Fah Luang chickens are required for comparison with Chinese black-boned chicken breeds to better understand how evolution and domestication occurred in these Thai local breeds.

4.2. Introgression of Red Junglefowl and Thai Domestic Chicken Breeds into Chee Fah and Fah Luang Chickens

Chee Fah and Fah Luang chicken breeds were hypothesized to have once encountered harsh environments, leading to the hybridization of red junglefowl or crossbreeding with other domestic chicken breeds before adapting to the Northern Thai environment. Their ancestral local chickens were bred in a free-range environment with low selection intensity, allowing them to hybridize with red junglefowl and/or native chickens in the neighborhood [43]. Based on microsatellite data, a few components of the gene pools of Chee Fah and Fah Luang chickens were shared with the gene pool of red junglefowl derived from Chiang Rai (the northern ecotype), Khao Kho (the northern and northeastern ecotype), Phetchaburi (the upper southern ecotype), and other domestic breeds, such as Mae Hong Son, Dong Tao, and Fighting chickens [28,29]. These results support our hypothesis that Chee Fah and Fah Luang chickens might have undergone a genetic introgression of red junglefowl or other domestic chickens in Thailand. The genetic footprint of the northeastern and upper southern ecotype of red junglefowl, and the northern ecotype as observed in Chee Fah and Fah Luang chickens may be a consequence of the large gene pools of red junglefowl across Thailand [28,29]. During over 50 years of domestication in complex and diverse ecological environments [44], Chee Fah and Fah Luang chickens have probably undergone genetic changes, admixture with other domestic chicken breeds, and the cultivation of specific conditions, thereby accumulating an abundance of genetic resources. Population structure analysis revealed that the Chee Fah and Fah Luang chicken populations formed an independent cluster that was different from those of red junglefowl and other Thai domestic chicken breeds. These local chicken breeds probably acquired unique and advantageous traits, such as ecological adaptability, during their process of domestication and population expansion. Interestingly, microsatellite genotyping showed that both Chee Fah and Fah Luang chickens shared the same gene pool at even different K-values, except for K = 25, although the external phenotypes, such as comb, hackle, and plumage color, were different between the two breeds [16]. This might result from the limited number of microsatellite markers, where the set of 28 microsatellite loci might not be enough to reflect the genetic divergence between the two breeds and can cause a bias due to the limited population examined. Larger sample sizes with a higher number of microsatellite markers are required to extensively investigate the evidence for the two genetically divergent breeds. Chinese indigenous black-boned chicken specimens are also required to extensively examine their gene pool and to delineate the genetic changes from the ancestral breeds of the Chee Fah and Fah Luang chickens.

4.3. Chee Fah and Fah Luang Chicken Breeds from Two Localities Show Different Population Structures, Different Gene Pool Origins, and Potential Signs of Adaptation to High Elevation

The Chee Fah and Fah Luang chickens from CRRBC shared the same allelic gene pool, but this was not the case for those from MLRBC. The external phenotypes are extensively different between Chee Fah and Fah Luang chickens [16], but both breeds from the same locality were clustered together at K = 25 in the results of the STRUCTURE, PCoA, and DAPC analyses. This concurred with the results of FST from both the microsatellite genotyping and mtDNA D-loop sequence data. Historically, the founders of the Chee Fah and Fah Luang chickens at MLRBC were captured from local communities in Chiang Rai in 2002 as the parental genetic stock, whereas the founders of the Chee Fah and Fah Luang chickens at CRRBC were collected from local communities in Chiang Rai in 2019. All samples used in this study were collected from the Research and Breeding Center of the Department of Livestock (Ministry of Agriculture and Cooperatives) after the possibility of genetic admixture of the ancestral Chee Fah and Fah Luang chickens, red junglefowl, and other domestic chickens had occurred. This suggests that at least two gene pool origins (from CRRBC and MLRBC) might remain in the Chee Fah and Fah Luang chicken populations independently. The allelic gene pool of the Chee Fah and Fah Luang chicken samples from MLRBC was lower in heterogeneity compared to that in those from CRRBC, possibly resulting from the large multiple mating generations of chicken breeds in MLRBC. Allelic changes between generations may be attributed to inbreeding, genetic drift, or even the sampling bias because the size of the individual populations of local chickens is relatively small (approximately 200 individuals) [44,45]. The levels of inbreeding or homozygosity appear to be higher over 10 years of establishment of the genetic stock [46] but can be reduced through the sire rotation scheme that is not currently used, as shown by the low FIS and high He values observed in the chickens in MLRBC. However, our genetic analyses using mtDNA D-loop sequences and microsatellite markers did not reveal any evidence of selective sweep in the Chee Fah and Fah Luang chickens. This might have resulted from the short period of time for the establishment of the Chee Fah and Fah Luang chickens. However, the possibility of the founder effect cannot be ruled out, which might have generated the similar patterns [47,48].
Surprisingly, a small part of the gene pool of the Chee Fah and Fah Luang chickens derived from MLRBC was shared with the Mae Hong Son chickens, with maintenance under the same environmental conditions (Mae Hong Son province), which is different from the Chee Fah and Fah Luang chickens in CRRBC (Chiang Rai province). Different environmental conditions between the Chiang Rai and Mae Hong Son provinces might have influenced the genetic composition of the Chee Fah and Fah Luang chicken populations. Habitat suitability model analyses showed the possibility that elevation is the key environmental factor for habitat suitability of the Chee Fah and Fah Luang chickens, which differed from the red junglefowl and the Mae Hong Son chickens [29; Wongloet et al., submitted data]. To confirm the level of landscape differences between the two areas, we compared environmental factors between chicken farms in Chiang Rai and Mae Hong Son provinces. Temperature, elevation, and precipitation (humidity) showed statistically significant differences between the two areas. This suggests that the Chee Fah and Fah Luang chickens derived from CRRBC might have been genetically differentiated under selective pressure due to niche environmental factors at high elevations, which also affected temperature and precipitation. By contrast, the Chee Fah and Fah Luang chickens derived from MLRBC might have adapted to the environment in Mae Hong Son. Identification of the signatures of adaptive evolution driven by different environments has become a key focus in evolutionary biology. As one such example, in the harshest environment in Tibetan Plateau at 2200–4100 m elevation, Tibetan domesticated chickens have developed effective strategies to survive at high altitudes through specific physiological and genetic adaptations that increase the number of red blood cells with a higher hemoglobin concentration to the low-oxygen (hypoxic) environment [48,49,50]. Large-scale physiological and genomic studies are thus required for Chee Fah and Fah Luang chickens to gather more conclusive evidence.
Genetic diversity among populations is generated by several genetic events, such as mutations, natural selection, genetic drift, and/or artificial selection [25,51,52]. In addition to analysis with a large number of samples using a higher number of microsatellite loci, the genome-wide analysis of single nucleotide polymorphism, and whole-genome sequencing are required to extensively investigate the adaptation process in Chee Fah and Fah Luang chickens from different localities. The findings obtained from such cross-sectional studies with chicken breeds collected from different geographic regions, such as highland and lowland areas in Northern Thailand, are also helpful for controlling the region-specific genetic properties of chickens that are adaptable to diverse environmental conditions. Exploring the selective signature mediated by climate change is critical for understanding the genetic basis of native environmental adaption in indigenous and local chickens, leading to making practical use of them as genetic resources in the future.

5. Conclusions

Indigenous and local chickens are globally used in farming, providing food security with low production costs and adaptability to harsh environmental conditions. Understanding their genetic diversity and adaptation to various environmental conditions is of practical value to human communities in the face of climate change. This study provides evidence for the origin and genetic footprint of local Chee Fah and Fah Luang chickens in Chiang Rai, Northern Thailand. Chee Fah and Fah Luang chickens possibly originated from Chinese indigenous black-boned chicken breeds, based on their genetic similarity in mtDNA D-loop sequences. Genetic footprints of red junglefowl and domestic chickens were observed in the Chee Fah and Fah Luang chickens as a consequence of hybridization and genetic introgression during the domestication process. These chicken breeds have useful genetic variations; therefore, further nutritional and genomic scans should be performed to identify new alleles/genes of agronomic importance.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su15086878/s1; Supplementary Data 1, Materials and Methods [28,29,30,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91]; Figure S1, Specimen origins (a) and phenotypic characteristics of male and female Chee Fah (b) and Fah Luang (c) Northern Thailand domestic chicken breeds; Figure S2, Study area and occurrence data of the Chee Fah and Fah Luang chickens; Figure S3, Environmental variables used to assess the species distribution model of the Chee Fah and Fah Luang chickens: (a) elevation, (b) distance to water, (c) normalized difference vegetation index (NDVI), (d) tree canopy cover, and (e) forest canopy height; Figure S4, Elevation (a,d), annual mean temperature (b,e), and annual precipitation (c,f) map with 466 local chicken farm stations from Mae Hong Son province and 918 local chicken farm stations from Chiang Rai province; Figure S5, Potential land suitability modeling of Chee Fah and Fah Luang chickens in Thailand; Figure S6, Maximum entropy modeling response area curves of the predictor variables influencing the Chee Fah and Fah Luang chicken distribution: (a) elevation, (b) forest canopy height, (c) main river, (d) normalized difference vegetation index (NDVI), and (e) tree cover; Figure S7, The Jackknife method used in maximum entropy modeling, and environmental factors affecting the potential distribution of Chee Fah and Fah Luang chickens; Figure S8, Environmental factor characteristics, including (a) mean and (b) histogram of elevation, (c) mean and (d) histogram of annual precipitation, and (e) mean and (f) histogram of annual temperature compared between Chiang Rai and Mae Hong Son provinces; Figure S9, Phylogenetic relationships among Chee Fah and Fah Luang, domestic breeds, and red junglefowl based on the maximum likelihood approach, with 10,000 ultrafast bootstrap replicates. The red dot represents samples from this study. The number above the node denotes bootstrap value. The letter and color indicate assigned haplogroups. Haplogroup nomenclature is based on Miao et al. [33]; Figure S10, Discriminant analysis of principal components (DAPC) and principal coordinate analysis (PCoA) results of (a,b) Chee Fah and (c,d) Fah Luang breeds from two populations (Mae Hong Son Livestock Research and Breeding Center (MLRBC) and Chiang Rai Livestock Research and Breeding Center (CRRBC)). Assigned genetic clusters are represented by different colors while dots represent different individuals; Figure S11, Different population structure patterns of Chee Fah (n = 20) and Fah Luang chickens (n = 19) generated by model-based Bayesian clustering algorithms implemented in STRUCTURE. (a) Plot of Evanno’s ΔK of Chee Fah chickens, (b) plot of Evanno’s ΔK of Fah Luang chickens, (c) plot of ln P(K) of Chee Fah chickens, and (d) Plot of ln P(K) of Fah Luang chickens; Figure S12, Population structure of (a) Chee Fah (n = 20) and (b) Fah Luang (n = 19) chicken individuals from two populations (Mae Hong Son Livestock Research and Breeding Center (MLRBC) and Chiang Rai Livestock Research and Breeding Center (CRRBC)). Each vertical bar on the x-axis represents an individual, while the y-axis represents the proportion of membership (posterior probability) in each genetic cluster. Black vertical lines indicate the boundaries. Detailed information on all indigenous chicken individuals is presented in Table S1; Figure S13, Mapping of expected heterozygosity (He) against inbreeding coefficients (FIS) along the length of the physical map. (a) Chee Fah chicken populations, (b) Fah Luang chicken populations, (c) microsatellite loci of the Chee Fah chickens and (d) microsatellite loci of the Fah Luang chickens; Figure S14, Discriminant analysis of principal components (DAPC) of Chee Fah and Fah Luang Chickens from Chiang Rai Livestock Research and Breeding Center (CRRBC) and Mae Hong Son Livestock Research and Breeding Center (MLRBC) with red junglefowl and domestic breeds. Scatter plots based on DAPC output for assigned genetic clusters are indicated by different colors. Dots represent different individuals; Figure S15, Different population structure patterns of Chee Fah (n = 20), Fah Luang (n = 19), red junglefowl, and domestic chicken breeds, generated by model-based Bayesian clustering algorithms implemented in STRUCTURE. (a) Plot of Evanno’s ΔK and (b) plot of ln P(K); Figure S16, Mapping of expected heterozygosity (He) against inbreeding coefficients (FIS) along the length of the physical map. (a) Chee Fah and Fah Luang chicken breeds, red junglefowl and domestic chicken breeds, and (b) microsatellite loci; Table S1, Representative specimens of two populations of Chee Fah and Fah Luang chicken breeds in Thailand. All mtDNA D-loop sequences were deposited in the DNA Data Bank of Japan (DDBJ); Table S2, Microsatellite primers and sequences of Chee Fah and Fah Luang chicken specimens; Table S3, Comparison of environmental factors at local chicken farms in Chiang Rai and Mae Hong Son provinces; Table S4, Genetic differentiation between two populations of Chee Fah and Fah Luang chickens in mitochondrial DNA D-loop sequence. Genetic differentiation coefficient (GST), Wright’s F-statistics for subpopulations within the total population (FST), ΦST from sequence data and haplotype data, average number of nucleotide substitutions per site between populations (Dxy), and net nucleotide substitutions per site between populations (Da). Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1.; Table S5, Pairwise differentiation of linkage disequilibrium of Chee Fah chicken individuals at Chiang Rai Livestock Research and Breeding Center (CRRBC) based on 28 microsatellite loci. Numbers indicate p-values with 110 permutations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S6, Pairwise differentiation of linkage disequilibrium of Chee Fah chicken individuals at Mae Hong Son Livestock Research and Breeding Center (MLRBC) based on 28 microsatellite loci. Numbers indicate p-values with 110 permutations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S7, Pairwise differentiation of linkage disequilibrium of Fah Luang chicken individuals at Chiang Rai Livestock Research and Breeding Center (CRRBC) based on 28 microsatellite loci. Numbers indicate p-values with 110 permutations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S8, Pairwise differentiation of linkage disequilibrium of Fah Luang chicken individuals at Mae Hong Son Livestock Research and Breeding Center (MLRBC) based on 28 microsatellite loci. Numbers indicate p-values with 110 permutations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S9, Genetic diversity of 39 individuals of Chee Fah and Fah Luang chicken breeds based on 28 microsatellite loci. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S10, Comparison of genetic diversity parameters between Chee Fah and Fah Luang chickens populations based on 28 microsatellite loci. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S11, Observed and expected heterozygosity of Chee Fah and Fah Luang chickens based on 28 microsatellite loci and genetic bottlenecks for all individuals. Data were calculated using Bottleneck version 1.2.02 [92]. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S12, Inbreeding coefficients and relatedness of Chee Fah and Fah Luang chicken breeds at the Chiang Rai Livestock Research and Breeding Center (CRRBC, Chiang Rai) and Mae Hong Son Livestock Research and Breeding Center (MLRBC, Mae Hong Son). Estimates were calculated using COANCESTRY version 1.0.1.9 [86] and GenAlEx version 6.5 [84]. Detailed information for all chicken individuals is presented in Table S1. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S13, Pairwise genetic differentiation (FST), pairwise FSTENA values with ENA correction for null alleles and RST values using FSTAT version 2.9.3 [81] of Chee Fah and Fah Luang chickens between populations based on 28 microsatellite loci. Numbers indicate p-values, with 110 permutations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S14, Pairwise genetic relatedness (r) for Chee Fah and Fah Luang Chickens in Chiang Rai and Mae Hong Son Livestock Research and Breeding Center (CRRBC) and Mae Hong Son Livestock Research and Breeding Center (MLRBC) populations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S15, Inbreeding coefficients (FIS) of 39 individuals of Chee Fah and Fah Luang chicken individuals in Chiang Rai Livestock Research and Breeding Center (CRRBC) and Mae Hong Son Livestock Research and Breeding Center (MLRBC) populations. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1; Table S16, Molecular variance (AMOVA) results for Chee Fah and Fah Luang chickens based on 28 microsatellite loci using Arlequin version 3.5.2.2 [70]. Detailed information on all of the Chee Fah and Fah Luang chicken individuals is presented in Table S1.

Author Contributions

Conceptualization, T.B., W.S., N.T.,and K.S.; formal analysis, T.B., N.T. and W.W. (Wongsathit Wongloet), A.C., N.A., T.T., P.W., T.P., S.F.A., A.L., N.M., R.C., M.N., K.H., T.S., Y.M. P.D., and K.S.; funding acquisition, K.S.; investigation, N.M., R.C., P.P., K.H., M.-S.P., J.-L.H. and K.S.; methodology, T.B., W.S., W.W. (Wongsathit Wongloet), N.A., W.T., W.W. (Wannapa Wannakan), A.M., P.W., T.P. and K.S.; project administration, K.S.; resources, W.C., S.P. and P.N.; supervision, T.S. and K.S.; validation, M.N. and K.S.; visualization, K.S.; writing—original draft, T.B., W.S., A.C. and K.S.; writing—review and editing, T.B., W.S., N.T., W.W. (Wongsathit Wongloet), A.C., N.A., W.T., W.W. (Wannapa Wannakan), A.M., T.T., P.W., T.P., S.F.A., A.L., N.M., R.C., P.P., M.N., W.C., K.H., S.P., T.S., M.-S.P., J.-L.H., Y.M., P.D., P.N. and K.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded in part by the High-Quality Research Graduate Development Cooperation Project between Kasetsart University and the National Science and Technology Development Agency (NSTDA) (6517400214) and (6417400247) awarded to TB, TP, TS, and KS, the NSTDA funds (NSTDA P-19-52238 and JRA-CO-2564-14003-TH) awarded to WS and KS, Kasetsart University Research and Development Institute funds (FF(KU)25.64) awarded to WS, SFA, and KS, a grant from Betagro Group (no. 6501.0901.1/68) awarded to KS, the Thailand Science Research and Innovation through the Kasetsart University Reinventing University Program 2021 (3/2564) awarded to TP, YM, AL, and KS, the Higher Education for Industry Consortium (Hi-FI) (6414400777) awarded to NA, the e-ASIA Joint Research Program (no. P1851131) awarded to WS and KS, and the Office of the Ministry of Higher Education, Science, Research, and Innovation. International SciKU Branding (ISB), Faculty of Science, Kasetsart University, awarded funds to WS and KS. No funding source was involved in the study design, collection, analysis, interpretation of the data, writing of the report, or the decision to submit the article for publication.

Institutional Review Board Statement

Experimental procedure and animal care approval for this study was granted by the Kasetsart University Animal Experiment Committee (Approval No: ACKU63-SCI-021 and ACKU63-SCI-022) and was conducted in accordance with the Regulations on Animal Experiments at Kasetsart University.

Informed Consent Statement

Not applicable.

Data Availability Statement

Mitochondrial DNA D-loop sequences generated in this study can be accessed at the DNA Data Bank of Japan (DDBJ) website (https://www.ddbj.nig.ac.jp/, accessed on 25 November 2022) (accession numbers: LC740526–LC740564). Microsatellite genotypic data and genotypic data of red junglefowl and Thai domestic chicken breeds/ecotypes can be accessed at the Dryad Digital Repository Dataset (https://doi.org/10.5061/dryad.hhmgqnkm0, accessed on 15 January 2023).

Acknowledgments

We thank the Mae Hong Son Livestock Research and Breeding Center, Mae Hong Son Provincial Livestock Office, and the Chiang Rai Livestock Research and Breeding Center, Chiang Rai Provincial Livestock Office, the Department of Livestock Development, the Ministry of Agriculture and Cooperatives, Thailand, for helping with the sample collection. We thank the Center for Agricultural Biotechnology (CAB) at Kasetsart University Kamphaeng Saen Campus and the NSTDA Supercomputer Center (ThaiSC) for support with server analysis services. We also thank the Faculty of Science (no. 6501.0901.1/71), the Faculty of Forestry of Kasetsart University, and the Betagro Group for providing research facilities.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Haplotype network based on sequence data for the mitochondrial DNA D-loop region of (a) Chee Fah chicken, (b) Fah Luang chicken, and (c) Chee Fah and Fah Luang chickens.
Figure 1. Haplotype network based on sequence data for the mitochondrial DNA D-loop region of (a) Chee Fah chicken, (b) Fah Luang chicken, and (c) Chee Fah and Fah Luang chickens.
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Figure 2. Principal component analysis (PCoA) of Chee Fah and Fah Luang chickens derived from Chiang Rai Livestock Research and Breeding Center (CRRBC) and Mae Hong Son Livestock Research and Breeding Center (MLRBC) with red junglefowl and domestic chicken breeds. Square indicates domestic chicken breeds. Triangle represents red junglefowl. Different population/breeds represented by different colors.
Figure 2. Principal component analysis (PCoA) of Chee Fah and Fah Luang chickens derived from Chiang Rai Livestock Research and Breeding Center (CRRBC) and Mae Hong Son Livestock Research and Breeding Center (MLRBC) with red junglefowl and domestic chicken breeds. Square indicates domestic chicken breeds. Triangle represents red junglefowl. Different population/breeds represented by different colors.
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Figure 3. Population structure of the Chee Fah, Fah Luang, red junglefowl, and domestic chicken breeds. Each vertical bar on the x-axis represents an individual chicken; the y-axis represents the proportion of membership (posterior probability) in each genetic cluster. Chee Fah, Fah Luang, red junglefowl, and domestic chicken breeds are superimposed on the plot, with black vertical lines indicating the boundaries. Detailed information on each domestic chicken is presented in Table S1.
Figure 3. Population structure of the Chee Fah, Fah Luang, red junglefowl, and domestic chicken breeds. Each vertical bar on the x-axis represents an individual chicken; the y-axis represents the proportion of membership (posterior probability) in each genetic cluster. Chee Fah, Fah Luang, red junglefowl, and domestic chicken breeds are superimposed on the plot, with black vertical lines indicating the boundaries. Detailed information on each domestic chicken is presented in Table S1.
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Table
Table 1. Mitochondrial DNA D-loop sequence diversity for Chee Fah and Fah Luang chicken breeds.
Table 1. Mitochondrial DNA D-loop sequence diversity for Chee Fah and Fah Luang chicken breeds.
BreedPopulationNNumber of Haplotypes (H)Theta (Per Site) from SAverage Number of Nucleotide
Differences (k)		Overall Haplotype (h)Nucleotide Diversities (π)
Chee FahMLRBC 11090.0043.6890.978 ± 0.0540.004 ± 0.00047
CRRBC 21080.0096.6440.933 ± 0.0770.007 ± 0.00144
Fah LuangMLRBC 110100.0117.6001.000 ± 0.0450.008 ± 0.00144
CRRBC 2980.0055.6110.972 ± 0.0640.006 ± 0.00103
Overall39180.008536.9590.994 ± 0.0190.007 ± 0.00083
1 Mae Hong Son Livestock Research and Breeding Center (MLRBC), Mae Hong Son; 2 Chiang Rai Livestock Research and Breeding Center (CRRBC), Chiang Rai.
Table
Table 2. Genetic diversity among 20 individuals of Chee Fah chickens and 19 individuals of the Fah Luang chickens based on 28 microsatellite loci.
Table 2. Genetic diversity among 20 individuals of Chee Fah chickens and 19 individuals of the Fah Luang chickens based on 28 microsatellite loci.
BreedPopulation Na1AR2Nea3I4Ho5He6PIC7F8
Chee FahMLRBC 9Mean3.7503.6762.5351.0070.6820.5490.498−0.208
S.E.0.2281.1630.1710.0710.0640.0350.1760.077
CRRBC 10Mean5.3935.2243.5251.3690.4410.6800.6350.350
S.E.0.3461.7120.2140.0710.0580.0250.1440.081
TotalMean4.5714.4503.0301.1880.5620.6140.5660.076
S.E.0.2331.6500.1510.0550.0460.0230.1740.067
Fah LuangMLRBC 9Mean4.8574.7033.0391.2080.6690.6170.569−0.092
S.E.0.3201.620.2410.0730.0580.0290.1550.078
CRRBC 10Mean5.1074.7653.6091.3420.4460.6690.628−0.092
S.E.0.3231.5350.2530.0780.0460.0320.1720.078
TotalMean4.9824.7343.3241.2750.5580.6430.5980.115
S.E.0.2261.5640.1770.0540.0400.0220.1650.056
1 Number of alleles (Na); 2 allelic richness (AR); 3 number of effective alleles (Nea); 4 Shannon’s information index (I); 5 observed heterozygosity (Ho); 6 expected heterozygosity (He); 7 polymorphic information content (PIC); 8 fixation index (F); 9 Mae Hong Son Livestock Research and Breeding Center (MLRBC), Mae Hong Son; 10 Chiang Rai Livestock Research and Breeding Center (CRRBC), Chiang Rai.
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Budi, T.; Singchat, W.; Tanglertpaibul, N.; Wongloet, W.; Chaiyes, A.; Ariyaraphong, N.; Thienpreecha, W.; Wannakan, W.; Mungmee, A.; Thong, T.; et al. Thai Local Chicken Breeds, Chee Fah and Fah Luang, Originated from Chinese Black-Boned Chicken with Introgression of Red Junglefowl and Domestic Chicken Breeds. Sustainability 2023, 15, 6878. https://doi.org/10.3390/su15086878

AMA Style

Budi T, Singchat W, Tanglertpaibul N, Wongloet W, Chaiyes A, Ariyaraphong N, Thienpreecha W, Wannakan W, Mungmee A, Thong T, et al. Thai Local Chicken Breeds, Chee Fah and Fah Luang, Originated from Chinese Black-Boned Chicken with Introgression of Red Junglefowl and Domestic Chicken Breeds. Sustainability. 2023; 15(8):6878. https://doi.org/10.3390/su15086878

Chicago/Turabian Style

Budi, Trifan, Worapong Singchat, Nivit Tanglertpaibul, Wongsathit Wongloet, Aingorn Chaiyes, Nattakan Ariyaraphong, Worawit Thienpreecha, Wannapa Wannakan, Autchariyapron Mungmee, Thanyapat Thong, and et al. 2023. "Thai Local Chicken Breeds, Chee Fah and Fah Luang, Originated from Chinese Black-Boned Chicken with Introgression of Red Junglefowl and Domestic Chicken Breeds" Sustainability 15, no. 8: 6878. https://doi.org/10.3390/su15086878

APA Style

Budi, T., Singchat, W., Tanglertpaibul, N., Wongloet, W., Chaiyes, A., Ariyaraphong, N., Thienpreecha, W., Wannakan, W., Mungmee, A., Thong, T., Wattanadilokchatkun, P., Panthum, T., Ahmad, S. F., Lisachov, A., Muangmai, N., Chuenka, R., Prapattong, P., Nunome, M., Chamchumroon, W., ... Srikulnath, K. (2023). Thai Local Chicken Breeds, Chee Fah and Fah Luang, Originated from Chinese Black-Boned Chicken with Introgression of Red Junglefowl and Domestic Chicken Breeds. Sustainability, 15(8), 6878. https://doi.org/10.3390/su15086878

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