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. 2023 Aug 25;102(12):103068. doi: 10.1016/j.psj.2023.103068

Phylogenetic analysis reveals multiple origins of Chinese gamecocks

Xufang Ren *, Zi Guan *, Haiying Li †, Li Zhang ‡, Junhui Wen *, Xiurong Zhao *, Gang Wang *, Xinye Zhang *, Huie Wang §, Fuqing Yu #, Zhihua Chen ||, Lujiang Qu *,§,1
PMCID: PMC10550403  PMID: 37778296

Abstract

Cockfighting is popular worldwide, dating back to 2,800 BC. Primarily, 5 modern Chinese gamecock breeds exist, located in the northeast (Luxi and Henan), west (Turpan), south (Xishuangbanna), and southeast (Zhangzhou) of China. However, whether Chinese gamecocks were derived from a single origin or multiple origins remains controversial. Therefore, this study used next-generation resequencing data to elucidate the origin of Chinese gamecocks by constructing genome-wide and SRY-box transcription factor 5 (SOX5) gene phylogenetic trees. Data from 161 chickens from 27 breeds, including 9 gamecock breeds, were included. Before constructing the SOX5 gene tree, we validated that the pea-comb phenotype mutation in all gamecock breeds was attributed to copy number variation in intron 1 of the SOX5 gene, as previously reported. The specific region was chr1: 65,838,000 to 65,846,000. The phylogenetic tree results suggested that Zhangzhou and Xishuangbanna gamecocks have a monophyletic origin, while Luxi, Henan, and Turpan gamecocks have a common ancestor. Our study provides genome-wide evidence that Chinese gamecocks have multiple origins and advances the understanding of the genetic mechanisms of the pea-comb characteristic.

Key words: Chinese gamecock, phylogenetic analysis, multiple origins

INTRODUCTION

Domestic chickens are an excellent and low-cost animal protein source for humans (Moazeni et al., 2016). Based on ancient DNA, the domestication of chickens dates back to as early as approximately 8,000 BC (Xiang et al., 2014). Now, Red Junglefowl (Gallus gallus) (RJF) from the jungles of south and southeast Asia is generally accepted as the wild progenitor of domestic chickens (Fumihito et al., 1994, 1996; Tixier-Boichard et al., 2011; Wang and Thakur, 2020). Besides the primary uses as broilers or layers, some domestic chickens have been used for cultural, religious, and entertainment purposes. Gamecocks are the products of cultivation by humans for cockfighting through long-term selection. Furthermore, different countries in Asia, such as China, Laos, Indonesia, and Thailand, all have separate gamecock breeds. However, unlike the origins of domestic chickens, the origin of gamecocks remains controversial.

In China, cockfighting dates back to 2,800 BC. Modern Chinese gamecock breeds are generally classified as Zhangzhou (ZZ), Turpan (Tur), Luxi (LX), Henan (HN), and Xishuangbanna (XSBN). Presently, 2 hypotheses exist to explain the domestication origin of Chinese gamecocks: 1) a monophyletic origin gave rise to all gamecock breeds, or 2) gamecock breeds were developed independently in different areas from wild or domestic chickens, thus, have multiple origins. Previous mitochondrial DNA (mtDNA)-based genetic studies raised the multiple origins hypothesis (Liu et al., 2006; Qu et al., 2009). However, separate mitochondrial genome analyses have limited potential for revealing complex past demography. In contrast, whole-genome phylogenetic analyses hold greater potential for investigating the evolutionary history of the domestication processes.

The pea-comb phenotype (Figure 1) is widespread among both European and Asian gamecock breeds, providing a smaller target for injury owing to its smaller size compared to other combs, such as a single-comb. Copy number variation in intron 1 of the SRY-box transcription factor 5 (SOX5) gene causes the pea-comb phenotype in chickens (Wright et al., 2009). Furthermore, the pea-comb mutation may have occurred during the early stages of gamecock domestication and was likely fixed at the origin. Therefore, the origin pattern of the pea-comb characteristic should be consistent with the domestication of gamecocks from different regions.

Figure 1.

Figure 1

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Single-comb (wild type) (A) and pea-comb (B) phenotypes in chickens.

The use of molecular techniques is essential and practical for characterizing breeds (Mousavizadeh et al., 2009; Jafari Ahmadabadi et al., 2023). Conservation of genetic diversity in animal species requires the proper performance of conservation superiorities and sustainable handling plans based on universal population structure information, including genetic diversity resources among and between breeds (Javanmard et al., 2008; Roudbar et al., 2018). Genetic diversity is essential for genetic improvements, population preservation, evolution, and environmental adaption (Mohammadi et al., 2009; Masoudzadeh et al., 2020). On the other hand, identifying gene polymorphism is important in farm animals breeding (Mohammadabadi et al., 2010, 2011) to define the animal's genotypes and their associations with productive, reproductive, and economic traits (Nassiry et al., 2005; Norouzy et al., 2005; Sulimova et al., 2007).

As mentioned, the origin of domestic Chinese gamecocks remains unclear. Clarifying the origin could allow better protection and utilization of these precious genetic resources. Furthermore, previous studies used mtDNA-based analyses, which are less accurate. Therefore, this study evaluated the evolutionary relationships and origin patterns of Chinese gamecocks by constructing genome-wide and SOX5 gene phylogenetic trees.

MATERIALS AND METHODS

Ethics Statement

This study was conducted following the guidelines for the experimental animals established by the Animal Care and Use Committee of China Agricultural University.

Sampling and Genome Sequencing

This study used 161 adult chickens, including 3 RJF, 76 chickens from China, 36 from Southeast Asia, 39 from Central Asia, and 7 from commercial breeds. In addition, the Chinese gamecock breeds (LX, ZZ, XSBN, Tur, and HN) were included, as were Balinese Game chickens (BL), a local breed used for cockfighting in Bali, Indonesia. Lari, the largest breed of Asil/Assel in Pakistan, Iran, and Afghanistan, and the Thailand (TH) Game chicken, an old breed originating in Thailand, were also included. Except for the commercial breeds, Rhode Island Red (RIR), Cornish (Cor), and White Leghorn (LH)), the remaining breeds were all indigenous chickens of the corresponding countries or regions. Table S1 provides detailed information on our samples.

Genomic DNA was extracted from fresh blood samples collected in EDTA-coated tubes using TIANamp Blood DNA Kit (Tiangen Biochemical Technology Co., Ltd., Beijing, China). Novogene Technology Co., Ltd. (Tianjin, China) determined the DNA concentration and quality, which passed their inspection. Then, next-generation resequencing was performed using the Illumina HiSeq 4000 sequencing platform (Illumina Inc., San Diego, CA). All raw data were checked before the analysis; low-quality reads and adaptors were filtered using fastp (v 0.23.2) (Chen et al., 2018) software with the default parameters.

Sequence Alignment and Single Nucleotide Polymorphism Calling

All clean reads were aligned independently against the chicken reference genome (galGal6) using the mem algorithm in the Burrows-Wheeler Aligner (v 0.7.17) software (Li and Durbin, 2010). The resulting files were then converted to bam format and sorted using Samtools (v 1.16.1) (Danecek et al., 2021). Subsequently, the duplicate reads created during the preparation of genomic libraries were marked and removed by the “MarkDuplicates” argument of Picard tools (2.52.2) (http://broad.institute.github.io/picard/). To improve the accuracy of downstream processing steps, local alignment and base quality recalibration of the sequences were performed using the “RealignerTargetCreator,” “IndelRealigner,” and “BaseRecalibrator” parameters in the Genome Analysis Toolkit (GATK) (v 3.8) (McKenna et al., 2010) software. Finally, single nucleotide polymorphism (SNP) calling was performed by the “Haplotypecaller” module under the default parameters.

The gvcf files of all individuals were merged using “GenotypeGVCFs” of GATK, while hard-filtering was performed by “VariantFiltration” with the option “–filterExpression ‘QUAL’ < 30.0 || QD < 5.0 || FS > 60.0 || MQ < 40.0 || MQRankSum < −12.5 || ReadPosRankSum < −8.0.” After secondary filtration by plink (v 1.9) (Purcell et al., 2007) software and the removal of SNPs on sex chromosomes, 12,370,429 variants and 157 chickens were obtained for subsequent study.

Location of Copy Number Variation in Intron 1 of SOX5

The SOX5 gene was used to build a phylogenetic tree and the premise is to ensure all gamecocks had the same pea-comb mutation. Thus, we verified whether copy number variation in intron 1 of SOX5 caused the pea-comb phenotype in all gamecocks in this study using Integrative Genomics Viewer genome visualization software (v 2.16.0) (Thorvaldsdóttir et al., 2013). We used this software to determine the specific location of the copy number variation in the SOX5 gene with relevant references (Bitgood et al., 1980; Bartlett et al., 1996; Wright et al., 2009).

Establishing Phylogenetic Trees

The SOX5 gene SNP (chr1: 65,531,053–66,179,027) were extracted from the merged vcf file using vcftools (v 0.1.16) (Danecek et al., 2011). A maximum likelihood (ML) tree for the SOX5 gene was then constructed using RAxML software (v 8.2.12) (Stamatakis, 2014). ML tree reconstruction based on whole-genome SNP was performed following the SNPhylo protocol (v 20180901) (Lee et al., 2014), with RJF as the outgroup. The phylogenetic trees were subsequently visualized using iTOL (Letunic and Bork, 2021). Treemix (v 1.13) software (Pickrell and Pritchard, 2012) was used to infer possible admixture events between breeds to better illustrate the relationships portrayed by the phylogenetic trees.

RESULTS

Validation of Copy Number Variation Regions in the SOX5 Gene

Based on previous research, we located the copy number variation regions on chromosome 1 from 65,838,000 to 65,846,000. The results suggested that all gamecock breeds in this study had the pea-comb shape. Single-comb breeds, such as RJF, LH, and RIR, did not carry the copy number variation (Figure 2A and B). Several unique individuals were also detected in gamecocks and indigenous chickens; Figure 2C presents the target region differences. Furthermore, Hetian (HT) 1 and HT2 displayed the same characteristics as gamecocks in the target region. The comb shape of Lari4 was identified as single-comb, while BL4 and BL6 had different characteristics to those of single- and pea-combs in the target region. Additionally, the BL4 and BL6 copy numbers were more than those of single-comb individuals, and the insertion and deletion of fragments were greater than pea-comb individuals.

Figure 2.

Figure 2

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Integrated Genomics Viewer visualization results of the copy number variation region in the SRY-box transcription factor 5 (i.e., SOX5) gene of Chinese gamecocks (A), foreign gamecock breeds (B), and some unique individuals (C). The gray shading of the target region represents read coverage.

Phylogenetic Analyses

Two ML trees were constructed using whole-genome SNP and the SOX5 gene to infer the phylogenetic relationships among all individuals (Figure 3).

Figure 3.

Figure 3

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Maximum likelihood phylogenetic tree of all breeds. Genome-wide phylogenetic tree (A). SRY-box transcription factor 5 (i.e., SOX5) gene phylogenetic tree (B).

In the genome-wide tree, 2 Thailand domestic chickens clustered (Thaliland1, Thailand2), as did 2 XSBN and 1 TH. Chickens from Thailand (TH gamecock), Indonesia (all BL, Indonesia1, and Indonesia2), and Laos (Laos3 and Laos5) clustered with all ZZ and 1 XSBN. Furthermore, gamecocks from central Asia (Lari) clustered individually, except Lari4, which clustered with 2 LH individuals. Additionally, gene flow was detected between Lari and LH (Figure S1). Chickens from Vietnam (all DT, Vietnam1, and Vietnam2) clustered with most of the XSBN gamecocks. Meanwhile, 3 other kinds of Chinese gamecocks (LX, Tur, and HN) clustered, except for LX2. Chinese indigenous chickens and 3 commercial breeds also clustered.

The clustering observed in the SOX5 gene tree was not completely consistent with the results above. First, Chinese indigenous chickens and 3 commercial breeds with the single-comb phenotype were separated from those with the pea-comb trait, except for Laos5. Five Chinese gamecock breeds were distributed on different branches, whereas ZZ gamecocks were distributed independently on a branch. Furthermore, 5 XSBN gamecocks (XSBN4, XSBN13, XSBN14, XSBN9, and XSBN10) were also separated from other Chinese gamecocks. All Tur, HN, and LX gamecocks were distributed in 2 branches, with several chickens from Southeast Asia and Central Asia being clustered with the 3 breeds.

DISCUSSION

Sequencing technology provides opportunities to dissect the domestication and history of various species from a more comprehensive perspective. For example, the origins of modern domestic chickens and geese (Wang and Thakur, 2020; Wen et al., 2023) have been determined using whole-genome sequencing data. In this study, we conducted a phylogenetic analysis based on whole-genome data to clarify the distinction between 5 Chinese gamecock breeds.

In the genome-wide tree, the HN, LX, and Tur breeds were clustered in a branch, suggesting they shared a common ancestor. However, individuals of these 3 breeds were separated into 2 branches in the SOX5 gene tree. Admixture between them may explain this result, which our previous study also suggested (Ren et al., 2023). LX2 clustered with several southern XSBN individuals, but we did not detect any gene flow between the LX and XSBN breeds. The LX1 and LX2 samples were collected from a part-time breeding farm; thus, the population size of this farm could have been too small. Consequently, the results are slightly less representative of the LX1 and LX2 populations.

Moreover, XSBN chickens were isolated from 4 other gamecock breeds and distributed across 2 branches of the genome-wide tree. Furthermore, several clustered with the Thailand or Laos gamecocks, while the others clustered with Vietnam chickens. This means that the modern XSBN gamecock may have different ancestors. This could be because Xishuangbanna is in Yunnan Province, the southernmost region of the Hengduan Mountains. The Yunnan Province borders Laos and Myanmar and is connected to Thailand and Vietnam via the Lancang-Mekong River. Thus, admixture could have occurred through communication between merchants and travelers. In addition, geographical distance could have separated XSBN gamecocks from the other 4 breeds.

The domestication history of ZZ gamecocks is shorter than the other 4 breeds, resulting in a different origin in the genome-wide and the SOX5 gene trees. In addition, the unique genetic background of ZZ gamecocks also emphasizes the uniqueness of this breed (Ren et al., 2023). The Fujian Province is home to ZZ gamecocks, which does not border any Southeast Asian countries and is far from the northern and central cities of China. Thus, its geographical location may also contribute to the uniqueness of this breed.

Finally, the similar clustering pattern of the 5 gamecock breeds across the 2 trees indicates an independent occurrence of pea-comb traits that synchronized with the formation and selection of breeds. In addition, we verified that the variation type generated in the SOX5 gene was the same in all gamecock breeds in this study. We also confirmed that Lari4 was a single-comb breed, and gene flow occurred between the Lari and LH breeds. Therefore, we hypothesized that the introgression between LH and Lari may have changed the comb shape of Lari4.

In conclusion, our results suggest that the pea-comb trait occurred independently among all gamecock breeds, synchronizing with the formation and selection of the breeds. Retaining the corresponding SOX5 genes also occurred independently. Similar distributions on the genome-wide and SOX5 gene phylogenetic trees indicate that ZZ and XSBN gamecocks have a monophyletic origin, but LX, HN, and Tur gamecocks have a common ancestor. Thus, our results suggest that Chinese gamecocks have multiple origins.

ACKNOWLEDGMENTS

This study was supported by High-performance Computing Platform of China Agricultural University. In addition, we want to thank Editage (www.editage.cn) for English language editing.

Funding: This study was supported by the Beijing Innovation Team of the Modern Agro-Industry Technology Research System for Poultry (BAIC06-2023-G01).

DISCLOSURES

The authors have no conflicts of interest to declare.

Footnotes

Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2023.103068.

Appendix. Supplementary materials

mmc1.docx (587.9KB, docx)

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