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. 2024 Apr 5;103(6):103694. doi: 10.1016/j.psj.2024.103694

Whole genome resequencing reveals genomic regions related to red plumage in ducks

Xinye Zhang *, Fangxi Yang †, Tao Zhu *, Xiurong Zhao *, Jinxin Zhang *, Junhui Wen *, Yalan Zhang *, Gang Wang *, Xufang Ren *, Anqi Chen *, Xue Wang ‡, Liang Wang §, Xueze Lv §, Weifang Yang §, Changqing Qu #, Huie Wang , Zhonghua Ning *, Lujiang Qu *,1
PMCID: PMC11068611  PMID: 38663207

Abstract

Plumage color is a characteristic trait of ducks that originates as a result of natural and artificial selection. As a conspicuous phenotypic feature, it is a breed characteristic. Previous studies have identified some genes associated with the formation of black and white plumage in ducks. However, studies on the genetic basis underlying the red plumage phenotype in ducks are limited. Here, genome-wide association analysis (GWAS) and selection signal detection (Fst, θπ ratio, and cross-population composite likelihood ratio [XP-CLR]) were conducted to identify candidate regions and genes underlying duck plumage color phenotype. Selection signal detection revealed 29 overlapping genes (including ENPP1 and ULK1) significantly associated with red plumage color in Ji'an Red ducks. ENSAPLG00000012679, ESRRG, and SPATA5 were identified as candidate genes associated with red plumage using GWAS. Selection signal detection revealed that 19 overlapping genes (including GMDS, PDIA6, and ODC1) significantly correlated with light brown plumage in Brown Tsaiya ducks. GWAS to narrow down the significant regions further revealed nine candidate genes (AKT1, ATP6V1C2, GMDS, LRP4, MAML3, PDIA6, PLD5, TMEM63B, and TSPAN8). Notably, in Brown Tsaiya ducks, GMDS, ODC1, and PDIA6 exhibit significantly differentiated allele frequencies among other feather-colored ducks, while in Ji'an Red ducks, ENSAPLG00000012679 has different allele frequency distributions compared with that in other feather-colored ducks. This study offers new insights into the variation and selection of the red plumage phenotype using GWAS and selective signals.

Key words: duck, selection signal detection, genome-wide association analysis, plumage color

INTRODUCTION

Bird plumage exists in various colors. In natural environments, plumage color diversity is usually associated with mating signals and camouflage adaptations to different surroundings. Similarly, human preferences for color have influenced poultry plumage coloration during selective breeding. Plumage color is primarily determined by melanin. Variations in color depths result from differences in the relative distribution and abundance of 2 types of melanin, that is, eumelanin (brown/black) and pheomelanin (yellow/red) (Serra, 1946). Melanin is synthesized within melanocytes. Variations in factors involved in the generation, migration, proliferation, and differentiation of melanocytes can impact melanin production, causing changes in plumage color (Yang et al., 2017; Huang et al., 2020; Hua et al., 2021).

Many genes influencing variation in plumage color phenotype have previously been identified. Extension/melanocortin-1 receptor (MC1R) is crucial in melanin synthesis, influencing various pigment deposition traits in mammals and bird species, including mice (Robbins et al., 1993), pigs (Kijas et al., 1998), sheep (Vage et al., 1999), chickens (Kerje et al., 2003), and ducks (Yu et al., 2013). The dominant white plumage color trait in chickens is associated with PMEL17, whereas the recessive white plumage color trait is related to TYR. In ducks, mutations and large intronic insertions in MITF cause the white plumage phenotype (Zhang et al., 2018; Zhou, et al., 2018). The mottled plumage color trait in chickens is caused by the EDNRB2 mutation (Kinoshita et al., 2014). Similarly, the dark-brown plumage color in chickens is caused by the deletion of a large upstream segment of SOX10 (Gunnarsson et al., 2011).

According to Chinese Poultry Genetic Resources, the Ji'an Red duck is a local specialty breed from Ji'an, Jiangxi, China, known for its red feathers, medium size, beautiful appearance, adaptability, and high egg production, which is cultivated into excellent raw material for plate duck after scientific and systematic selection and breeding. It has wide application prospects. The Brown Tsaiya duck is from Taiwan, China, and is characterized by its light brown feathers, small body size, and high egg production. However, studies on the genetic basis of red/light brown plumage color phenotypes in ducks are limited. Analyzing the reasons for the formation of their plumage color can provide a rational basis for selecting breeds and marking-assisted selection of Ji'an Rd and Brown Tsaiya ducks. Here, we reported the whole genome sequences of 18 red-feathered ducks, including 10 Brown Tsaiya and 8 Ji'an Red. We conducted a genome-wide association study (GWAS) and selection signal detection to identify candidate genes and regions associated with the red plumage color trait in ducks by integrating these data with our previously obtained and 13 publicly available samples. This study contributed to advancing our understanding of the duck plumage color genetics, thereby helping to improve varieties.

MATERIALS AND METHODS

We collected 103 ducks from 12 different breeds. The Brown Tsaiya and Ji'an Red ducks were obtained from the Taiwan and Fujian Provinces (China), respectively. The remaining duck samples were obtained from our previous studies (Zhang et al., 2018; Zhu et al., 2021; Zhang et al., 2023b). We downloaded 13 sets of sequencing data from NCBI. Their detailed information (including breed names, plumage color phenotypes, sampling locations, and primary sequence accession numbers) is presented in Table 1 and Table S1. Blood samples were collected through standard venipuncture. Genomic DNA was extracted using the TIANamp Genomic DNA Kit (TIANGEN Biotech, Beijing, China), according to the manufacturer's instructions. DNA concentration and quality were detected using NanoDrop. For genome sequencing, 2 paired-end libraries with an insert size of 500 bp were constructed and sequenced using the Illumina HiSeq 2500 platform. The average raw read sequence coverage of the duck population is 5x. The animal experimentation protocols were approved by the Animal Welfare Committee of China Agricultural University (permit XK622, Permit 046/2018), and the study was performed following ethical guidelines for animal research.

Table 1.

Summary of individuals used in this study.

Breed Abbreviation Sample size Geographic origin Phenotype Sample origin
Ji'an Red duck JAN 13 This study; Jiang et al., 2021; Zhou et al., 2018 red Jiangxi, China
Brown Tsaiya duck HC 10 This study light brown Taiwan, China
Wendeng Black duck WD 8 Zhang et al., 2023b black Shandong, China
Putian Black duck PT 8 Zhang et al., 2023b black Fujian, China
Longsheng-Cui duck LONGS 8 Wang et al., 2021 black Guangxi, China
Spot-billed duck BZ 8 Zhu et al., 2021 hemp Ningxia, China
Mallard MD 8 Zhang et al., 2018 hemp Zhejiang, China
Gaoyou duck GY 8 Zhang et al., 2018 hemp Jiangsu, China
Jinding duck JD 8 Zhang et al., 2018 hemp Fujian, China
Mei duck MEI 8 Zhu et al., 2021 hemp Anhui, China
Shanma duck SM 8 Zhang et al., 2018 hemp Fujian, China
Shaoxing duck SX 8 Zhang et al., 2018 hemp Zhejiang, China
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Alignments and Variant Identification

The raw data were filtered using default parameters using fastp (v0.20.0) (Chen et al., 2018) to avoid low-quality reads. All cleaned reads were aligned to the duck reference genome (cau_duck1.0) using BWA-MEM (v0.7.15) (Li and Durbin, 2009). The Genome Analysis Toolkit (GATK v4.1.8.1) (McKenna et al., 2010) was used for the realignment of reads and SNP calling. The ’SortSam’ command of GATK was used to convert the alignment results to the bam format and read sorting by coordinate. We performed quality control on the generated variant set using the default GATK parameters, retaining only high-quality SNP. Single nucleotide polymorphisms were filtered using the following standards: (a) QUAL > 30.0, (b) QualByDepth (QD) > 5.0, (c) FisherStrand (FS) < 60.0, (d) RMS MappingQuality (MQ) > 40.0, (e) MappingQualityRankSunTest (MQRankSum) > -12.5, and (f) ReadPosRankSum > -8.0. Finally, 11,938,694 SNP were retained for the subsequent association analysis.

Population Structure Analysis

Plink (v1.9) (Chang et al., 2015) was used for principal components analysis (PCA) to generate eigenvectors and eigenvalues. The first 2 principal components were selected as the x and y coordinates, and the data were visualized using the plot function in R.

Genome-Wide Selective Sweep Analysis

Selective sweeps between populations with red and other plumage colors were detected using Fst, θπ ratio, and cross-population composite likelihood ratio (XP-CLR). The Fst value and θπ ratio were calculated with 10-kb windows and slides with 5-kb steps using VCFtools (v0.1.13) (Danecek et al., 2011). XP-CLR was calculated with 10-kb windows and slides with 5-kb steps. In each approach, windows within the top 1% values were considered significant. Overlapping windows within the top 1% values of Fst, θπ ratio, and XP-CLR were simultaneously regarded as candidate selection regions.

GWAS

A univariate mixed linear model in GEMMA (v0.98.1) (Zhou and Stephens, 2012) was used to identify SNPs significantly associated with plumage color phenotype traits. The models are as follows:

y=Wα+xβ+u+ϵ

where y denotes the vector of phenotypic values for individuals, W is the matrix of covariates, α denotes the vector of corresponding coefficients comprising the intercept, x is the vector of marker genotypes, β is an estimate of the marker/SNP additive effect, u is the vector of random effects, and ϵ is the vector of errors. The Manhattan and Quantile-Quantile plots were drawn using the R package “CMplot” package.

Candidate Gene Analysis

We used Ensembl (http://www.ensembl.org/biomart/martview/) for gene annotation. Metascape (https://metascape.org/gp/index.html) was used for the biological function and relevant pathway analyses. Beagle (v5.4) software (Browning et al., 2018) was used to construct haplotypes within the target regions. Additionally, allele frequencies and π statistics were calculated to verify the candidate sweep regions.

RESULTS

Population Structure

PCA showed a distinct stratification between domesticated breeds and wild populations based on the first principal components (PC1). Additionally, a distinct separation was observed between brown mallards and domestic duck populations based on the second principal components (PC2) (Figure 1).

Figure 1.

Figure 1

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Principal components analysis (PCA) plot of duck populations in this study Each color represents a breed, and the abbreviations are as defined in Table 1.

Association Analysis of Red Plumage Phenotype in Ji'an Red Ducks

Selecting Plumage Color Traits

To identify the selection signature associated with red plumage, we searched the duck genome for regions using 3 statistical methods (Fst, π ratio, and XP-CLR) to compare the populations of red (JAN) and non-red (MD, BZ, JD, SX, GY, SM, MEI, WD, PT, and LONGS) plumage ducks based on sliding 10-kb windows with 5-kb steps (Figure 2). The regions within the top 1% values were considered candidate genomic regions. We identified 227, 305, and 538 candidate genes through Fst, π-ratio, and XP-CLR, respectively. On combining Fst, π ratio, and XP-CLR analyses, we identified 29 overlapping selected genes, including DCN, ENPP1, ESRRG, FGD4, GALNT1, GALNTL6, HAPLN1, RASSF6, RIMKLB, SKAP1, SLC25A21, SPAG16, SPATA5, SRGAP1, TPK1, and ULK1 (Table 2). In our list of overlapping selected genes, ENPP1 and ULK1 were notable owing to their association with pigment deposition.

Figure 2.

Figure 2

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Selective signals of red plumage color in Ji'an Red duck. (A) Genome wide distribution of Fst. (B) Genome wide distribution of θπ ratio. (C) Genome wide distribution of XP-CLR. (D) Fst, θπ ratio, and XP-CLR screened for overlapping genes.

Table 2.

Overlapping significant regions identified through Fst, pi, and cross-population composite likelihood ratio (XP-CLR) and associated genes in Ji'an red duck.

Gene Full Name Chromosome Location (bp)1 Length (bp)1 Number (SNP)2
FLT1 Fms-related receptor tyrosine kinase 1 1 140607629-140714774 107145 0
SRGAP1 SLIT-ROBO Rho GTPase activating protein 1 1 34632585-34784998 152413 0
DCN Decorin 1 47576720-47618330 41610 0
FGD4 FYVE, RhoGEF and PH domain containing 4 1 61408749-61520984 112235 0
A2ML1 alpha-2-macroglobulin like 1 1 78744053-78759702 15649 0
RIMKLB Ribosomal modification protein rimK like family member B 1 78809659-78868404 58745 0
PIEZO2 Piezo-type mechanosensitive ion channel component 2 2 108182771-108436216 253445 0
TPK1 Thiamin pyrophosphokinase 1 2 56610690-56924039 313349 0
GALNT1 Glycine receptor alpha 3 2 88805150-88885411 80261 0
ESRRG Estrogen-related receptor gamma 3 19239319-19591403 352084 2
ENPP1 Ectonucleotide pyrophosphatase/phosphodiesterase 1 3 59439252-59495836 56584 0
APBB2 Amyloid beta precursor protein binding family B member 2 4 41121623-41293764 172141 0
LIMCH1 LIM and calponin homology domains 1 4 41347255-41516480 169225 0
RASSF6 Ras association domain family member 6 4 46531424-46545165 13741 0
SPATA5 Spermatogenesis associated 5 4 50364115-50553393 189278 2
GALNTL6 Polypeptide N-acetylgalactosaminyltransferase like 6 4 67885840-68340827 454987 0
GLRA3 Glycine receptor alpha 3 4 69037780-69126058 88278 0
EHD4 EH domain containing 4 5 30785990-30809368 23378 0
SLC25A21 Solute carrier family 25 member 21 5 38842670-39100823 258153 0
SPAG16 Sperm-associated antigen 16 7 7830019-8217436 387417 0
ULK1 Unc-51-like autophagy activating kinase 1 16 2432092-2511157 79065 0
CA10 Carbonic anhydrase 10 19 8107861-8307451 199590 0
SKAP1 Src kinase-associated phosphoprotein 1 28 4928465-5045546 117081 0
CCBE1 Collagen and calcium binding EGF domains 1 Z 12928073-13020979 92906 0
CELF4 CUGBP Elav-like family member 4 Z 2270219-2590923 320704 0
SYK Spleen-associated tyrosine kinase Z 47469844-47525435 55591 0
HAPLN1 Hyaluronan and proteoglycan link protein 1 Z 75004898-75063923 59025 0
FAM172A Family with sequence similarity 172 member A Z 79206564-79452504 245940 0
ADGRV1 Adhesion G protein-coupled receptor V1 Z 80535623-80810901 275278 0
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1

Source: Reference cau_duck1.0 primary assembly (Ensembl).

2

The number of genomes significant SNP located in gene identified in genome-wide association analysis

GWAS for Plumage Color Traits

Subsequently, we used the red plumage group as the case and the non-red group as the control and performed GWAS to identify candidate genes that influence the plumage color traits in Ji'an Red ducks (Figure 3). We found 3 significant peaks on chromosomes 3, 10, and 21, with 418 significant SNPs. Ensembl was used to annotate significant SNPs. Fifty-five genes were identified around significant peaks. The most significant SNP (chr10: 15076449; −log10p = 16.88) was in ENSAPLG00000012679. ESRRG and SPATA5 overlap within the top 1% windows detected in the selection signal scan of Ji'an Red ducks against other non-red-feathered duck populations, prompting more comprehensive future studies.

Figure 3.

Figure 3

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Genome-wide association study for red plumage color in Ji'an Red duck. (A) Manhattan plot of genome-wide association study. (B) Quantile–quantile (Q–Q) plots from the genome-wide association analysis (GWAS).

Analyzing Candidate Genes

The genomic architecture of the candidate genes in different plumage populations was analyzed by calculating the allele frequency. Notably, ENSAPLG00000012679 exhibited significant differences in allele frequency between Ji'an Red ducks and other plumage populations (Table S2), as verified in the haplotype comparison analysis (Figure 4).

Figure 4.

Figure 4

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Haplotype and nucleotide diversities in ENSAPLG00000012679 regions. (A) Heatmap in ENSAPLG00000012679 regions. (B) Nucleotide diversity in ENSAPLG00000012679 regions. Red represents Ji'an Red duck; blue represents ducks with other plumage color.

Association Analysis of Red Plumage Phenotype in Brown Tsaiya Ducks

Selecting Plumage Color Traits

To identify the selection signature associated with red plumage in Brown Tsaiya ducks, we employed the same methods that were used in Ji'an Red ducks (Figure 5). We identified 253, 371, and 490 candidate genes through Fst, π-ratio, and XP-CLR, respectively. On combining Fst, π ratio, and XP-CLR analyses, we identified 19 overlapping selected genes (AKT1, ARHGAP15, ATP6V1C2, CCDC149, FNTA, GMDS, ITGB1BP1, LRFN2, LRP4, LY75, MAML3, ODC1, PDIA6, PEX5L, PLD5, RBPJ, SLC4A7, TMEM63B, and TSPAN8) (Table 3). These genes are potentially associated with light brown plumage color in Brown Tsaiya ducks. In our overlapping selected gene list, GMDS, PDIA6, and ODC1 were notable owing to their association with pigment deposition.

Figure 5.

Figure 5

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Selective signals of red plumage color in Brown Tsaiya ducks. (A) Genome wide distribution of Fst. (B) Genome wide distribution of θπ ratio. (C) Genome wide distribution of XP-CLR. d. Fst, θπ ratio, and XP-CLR screened for overlapping genes.

Table 3.

Overlapping significant regions identified through Fst, pi, and cross-population composite likelihood ratio (XP-CLR) and associated genes in Brown Tsaiya ducks.

Gene Full name Chromosome Location (bp)1 Length (bp)1 Number (SNP)2
TSPAN8 Tetraspanin 8 1 37426355-37505746 79391 2
SLC4A7 Solute carrier Family 4 Member 7 2 40756860-41023690 266830 0
GMDS GDP-mannose 4,6-dehydratase 2 79265182-79671011 405829 67
LRFN2 Leucine-rich repeat and fibronectin type III domain containing 2 3 31578187-31799373 221186 0
TMEM63B Transmembrane protein 63B 3 33884914-33910150 25236 9
PLD5 Phospholipase D family member 5 3 39264361-39411447 147086 1
PDIA6 Protein disulfide isomerase family A member 6 3 76340827-76361379 20552 1
ATP6V1C2 ATPase H+ transporting V1 subunit C2 3 76352052-76370640 18588 1
ODC1 Ornithine decarboxylase 1 3 76457110-76500422 43312 0
ITGB1BP1 Integrin subunit beta 1 binding protein 1 3 77064448-77071033 6585 1
CCDC149 Coiled-coil domain containing 149 4 35632538-35680171 47633 0
RBPJ Recombination signal binding protein for immunoglobulin kappa J region 4 35946940-36092637 145697 0
MAML3 Mastermind like transcriptional coactivator 3 4 56585225-56781405 196180 10
LRP4 LDL receptor-related protein 4 5 32874741-32912588 37847 27
AKT1 AKT serine/threonine kinase 1 5 55272740-55337060 64320 16
LY75 Lymphocyte antigen 75 7 20553853-20598781 44928 0
ARHGAP15 Rho GTPase activating protein 15 7 31076813-31407565 330752 0
PEX5L Peroxisomal biogenesis factor 5 like 9 18643390-18680809 37419 0
FNTA Farnesyltransferase, CAAX box, alpha Z 52676230-52686816 10586 0
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1

Source: Reference cau_duck1.0 primary assembly (Ensembl).

2

The number of genomes significant SNP located in gene identified in genome-wide association analysis.

GWAS for Plumage Color Traits

GWAS was performed in Brown Tsaiya ducks to further support results from the selection sweep analysis (Figure 6). There were 3 significant peaks on chromosomes 1, 3, and 11, with 2,224 significant SNPs. Among the significant SNPs, 197 candidate genes were annotated. The most significant SNP (chr11: 1844022; −log10p = 57.32) was in AP4E1. Additionally, AKT1, ATP6V1C2, GMDS, LRP4, MAML3, PDIA6, PLD5, TMEM63B, and TSPAN8 were annotated and overlapped within the top 1% windows detected in the selection signal scan of Brown Tsaiya ducks against other non-red-feathered duck populations. Similarly, 2 overlapping genes associated with pigment deposition (PDIA6 and GMDS) were identified using GWAS and selection signal detection and require focus.

Figure 6.

Figure 6

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Genome-wide association study for red plumage in Brown Tsaiya ducks. (A) Manhattan plot of genome-wide association study. (B) Quantile–quantile (Q–Q) plots from the genome-wide association analysis (GWAS).

Analyzing Candidate Genes

We calculated the allele frequency differences between Brown Tsaiya and other duck breeds with respect to these significant genes and observed that GMDS, ODC1, and PDIA6 exhibited significant differences between Brown Tsaiya and other duck breeds (Tables S3, S4, and S5); the same was verified in the haplotype comparison analysis (Figure 7; Figures S1 and S2).

Figure 7.

Figure 7

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Haplotype and nucleotide diversities in PDIA6 regions. (A) Heatmap in PDIA6 regions. (B) Nucleotide diversity in PDIA6 regions. Red represents the Brown Tsaiya duck; blue represents ducks with other plumage color.

DISCUSSION

During extended domestication and breeding processes, Ji'an Red and Brown Tsaiya ducks exhibit distinct plumage color phenotypes (red/light brown). Ji'an Red and Brown Tsaiya ducks are among the few domestic duck breeds characterized by their red plumage, that holds substantial cultural and economic significance. Therefore, studying candidate genes associated with plumage color traits is essential. Natural and artificial selection significantly influences the genome during animal domestication. Rapidly advancing sequencing technologies provided greater convenience for studying genetic variations associated with phenotypes. In this study, we performed GWAS and selection sweep analysis using SNPs derived from whole genome sequencing on 103 duck samples and identified candidate genes associated with the red plumage phenotype.

In Ji'an Red ducks, we analyzed the genetic basis of the red plumage trait through selection signal analysis and GWAS and identified 19 overlapping genes. Among these genes, ENPP1 (encoding ectonucleotide pyrophosphatase/phosphodiesterase 1) and ULK1 were associated with pigment deposition. The somatomedin-B-like 2 (SMB2) domain of ENPP1 affects epidermal pigmentation and differentiation (Eytan et al., 2013). A missense mutation in ENPP1 can reportedly induce the development of hyperpigmented lesions with hypopigmented macules, causing a hereditary skin disorder (Chourabi et al., 2018). ULK1 regulated melanin levels, where its depletion increased TYR and MITF transcriptions (Ho et al., 2011; Kalie et al., 2013). In addition to the candidate genes associated with pigmentation, ENPP1 and ULK1, 2 other overlapped genes were detected through GWAS, ESRRG, and SPATA5. ESRRG is involved in steroid hormone-mediated signaling pathway and is essential in the development of the renal papilla (Berry et al., 2011). SPATA5 correlates with brain development (Buchert et al., 2016; Tanaka et al., 2015). Other candidate genes were related to growth and development, the nervous system, and fat deposition. The mechanism underlying red plumage is unknown in ducks. We speculated that these genes may influence the development of the red plumage phenotype in Ji'an Red ducks; however, their precise mechanisms of action remain unclear.

We performed selection signal detection (including Fst, θπ ratio, and XP-CLR) on Brown Tsaiya ducks and identified 19 overlapped genes with diverse functions, indicating that plumage color is a complex multifactorial trait. Among the candidate genes, those associated with pigment deposition include GMDS, PDIA6, and OCD1. GMDS is associated with pigmentation traits in chickens (Nie et al., 2016) and is related to the non-white wool trait in sheep (Zhang et al., 2023a). PDIA6 is a member of the protein disulfide isomerase family that activates the Wnt/β-catenin pathway (Gao et al., 2016). The Wnt/β-catenin signaling pathway plays a crucial role in melanogenesis (Liu et al., 2023). PDIA6 is a candidate gene for pigmentation in East Asian populations (Hider et al., 2013). Increased ODC1 levels induce elevated putrescine levels, promoting the generation of TYR (tyrosinase) and facilitating melanin synthesis in human skin (Sridharan et al., 2020). Other candidate genes had multiple functions. TSPAN8, LRFN2, PLD5, ATP6V1C2, ITGB1BP1, CCDC149, MAML3, LY75, and ARHGAP15 correlate with disease (Pan et al., 2015; Onishi et al., 2018; Takagi et al., 2018; Jobst-Schwan et al., 2020; Shah et al., 2020; Verma et al., 2020; Liu et al., 2021; Kessler et al., 2022; Lee et al., 2022; Li et al., 2022; Zhou et al., 2022; Ahmad et al., 2023). SLC4A7 is related to purine and pyrimidine nucleotide biosynthetic processes (Ali et al., 2022). TMEM63B is associated with ion channel activity (Marques et al., 2019; Du et al., 2020). RBPJ is related to angiogenesis (Jiang et al., 2022) and somitogenesis (Shi and Stanley, 2003; Ferjentsik et al., 2009). LRP4 is associated with the development of the nervous system (Shen et al., 2015; DePew and Mosca, 2021). AKT1 is associated with carbohydrate and glucose metabolism (Toda et al., 2020; Wu et al., 2023). PEX5L is related to adipogenesis (Guo et al., 2021). FNTA correlates with protein farnesyltransferase activity (Wang et al., 1996). Among the overlapping genes identified through the selection signal scan analysis, AKT1, ATP6V1C2, GMDS, LRP4, MAML3, PDIA6, PLD5, TMEM63B, and TSPAN8 were detected through GWAS. Notably, GMDS and PDIA6 are markedly associated with pigment deposition in both analysis. Haplotype analysis indicates that the 2 genes allow for a significant differentiation between Brown Tsaiya ducks and those with other plumage colors. Furthermore, there were significant differences in the genotype frequencies for GMDS and PDIA6; however, the SNPs were in the intronic regions. Given the roles of these genes in pigment deposition, it was hypothesized that the genetic basis of the red plumage phenotype is complex, possibly involving multiple genes.

In the Brown Tsaiya and Ji'an Red ducks, distinct significant peaks were not detected in the red/white group of the association analysis. This could be attributed to the influence of interactions among genes or the hierarchical dominance order of feather colors in ducks, with white feathers exhibiting precedence over red feathers. Hence, gene effects may not be detectable at the genomic level.

In this study, we performed selection signal scans (using methods such as Fst, θπ ratio, and XP-CLR) to identify selection signatures. We simultaneously conducted an association mapping analysis to investigate the genetic basis of the red plumage phenotype. GWAS was designed based on a case-control approach, comparing red plumage color ducks to different plumage color ducks. This design facilitated the precise localization of candidate genes influencing plumage color through overlap between multiple methods.

However, there were some limitations that could introduce ambiguity in interpreting the selected signals. The overlapping genes identified in our analysis may be associated with the distinction between red plumage and other phenotypes and with signals of breed-specific selection that occurred during the domestication process, potentially related to other traits. Further studies are required to validate these candidate genes.

The study revealed potential candidate genes involved in the formation of the red plumage phenotype in duck populations. Specifically, ENSAPLG00000012679, ENPP1, ULK1, GMDS, PDIA6, and ODC1 were the candidate genes associated with the formation of the red plumage phenotype in ducks. This study contributes to a deeper understanding of the duck plumage color genetics, highlighting the complexity of the trait's formation and providing new insights into the variation and selection of the red plumage phenotype in Ji'an Red ducks and Brown Tsaiya ducks, which is essential for breeding purposes.

ACKNOWLEDGMENTS

This work was supported by the Beijing Agriculture Innovation Consortium [grant numbers BAIC06-2023] and supported by the High-performance Computing Platform of China Agricultural University.

DISCLOSURES

The authors declare no conflicts of interest.

Footnotes

Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2024.103694.

Appendix. Supplementary materials

mmc1.xlsx (61KB, xlsx)
mmc2.pdf (55.6MB, pdf)

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