- Research Article
- Open Access
Detection of copy number variations in brown and white layers based on genotyping panels with different densities
© The Author(s) 2018
- Received: 7 May 2018
- Accepted: 23 October 2018
- Published: 6 November 2018
Copy number variations (CNV) are an important source of genetic variation that has gained increasing attention over the last couple of years. In this study, we performed CNV detection and functional analysis for 18,719 individuals from four pure lines and one commercial cross of layer chickens. Samples were genotyped on four single nucleotide polymorphism (SNP) genotyping platforms, i.e. the Illumina 42K, Affymetrix 600K, and two different customized Affymetrix 50K chips. CNV recovered from the Affymetrix chips were identified by using the Axiom® CNV Summary Tools and PennCNV software and those from the Illumina chip were identified by using the cnvPartition in the Genome Studio software.
The mean number of CNV per individual varied from 0.50 to 4.87 according to line or cross and size of the SNP genotyping set. The length of the detected CNV across all datasets ranged from 1.2 kb to 3.2 Mb. The number of duplications exceeded the number of deletions for most lines. Between the lines, there were considerable differences in the number of detected CNV and their distribution. Most of the detected CNV had a low frequency, but 19 CNV were identified with a frequency higher than 5% in birds that were genotyped on the 600K panel, with the most common CNV being detected in 734 birds from three lines.
Commonly used SNP genotyping platforms can be used to detect segregating CNV in chicken layer lines. The sample sizes for this study enabled a detailed characterization of the CNV landscape within commercially relevant lines. The size of the SNP panel used affected detection efficiency, with more CNV detected per individual on the higher density 600K panel. In spite of the high level of inter-individual diversity and a large number of CNV observed within individuals, we were able to detect 19 frequent CNV, of which, 57.9% overlapped with annotated genes and 89% overlapped with known quantitative trait loci.
Copy number variations (CNV) refer to large-scale insertions, duplications, or deletions of DNA sequence segments compared to a reference assembly. CNV can range in size from 50 to millions of base pairs, but 1 kb is generally assumed to be the lower limit [1, 2]. Most genome-wide mapping studies of CNV have been conducted in humans, where CNV account for a significant proportion of genome variation and are associated with susceptibility to disease [2–5]. According to Zarrei et al. , 4.8 to 9.5% of the human genome consists of CNV, while other studies in human and mouse found that CNV explained 18 to 30% of the genetic variation in gene expression [7, 8].
A better understanding of CNV in domesticated animal genomes will contribute to greater genetic improvement of production traits and animal health . Several species of farm animals have been scanned for CNV, including cattle [10–12], sheep [13, 14], goats , and pigs [16–18] and numerous studies have examined CNV in the chicken genome [19–32]. Currently, the known CNV in chicken encompass approximately 8.3% of its genome, or 9.6% of the ordered genome assembly . A number of other avian species have also been scanned for CNV, including duck  and turkey . Skinner et al.  have analyzed CNV in 16 species of birds and found that the number of CNV per Mb was similar in birds and mammals but that their size was smaller in birds than in mammals. In addition, overlapping between CNV and genes in chicken seems to be at the higher end of the range observed in mammals , which suggests that CNV may have functional effects in chickens.
According to studies on the human genome, formation of CNV can be connected to differences in recombination rate across the genome [35, 36]. Based on this hypothesis, recombination hot spots should have a higher prevalence of CNV than other parts of the genome. Indeed, based on an analysis of the genomes of chicken and zebra finch, Völker et al.  found a significant association between presence of structural variations such as chromosomal rearrangements and recombination rate. These data suggest a major role of recombination-based processes in the evolution of avian genomes.
Copy number variations can be detected by a number of methods, including array comparative genome hybridization (aCGH), sequencing, and single nucleotide polymorphism (SNP) arrays . Although SNP arrays are designed primarily for SNP genotyping, detection of CNV is possible because of the abnormal hybridization that occurs when a SNP is located within a CNV region. In general, the use of a 60K SNP  chip for this purpose has resulted in low frequencies of detected CNV [22, 29]. The use of sequence data is much more efficient and yields the largest number of CNV detected [24, 26, 27], but using a 600K SNP array can increase the sensitivity of CNV detection significantly . Four CNV detection studies based on the high-density Affymetrix 600K SNP array have been reported in chicken [28, 30–32] and have shown that, in general, CNV detection with this panel is more efficient than with lower density SNP chips.
Our study aimed at (1) detecting CNV and refining the genome-wide copy number profiles for layer chickens; (2) comparing CNV detection across different SNP genotyping panels, in order to evaluate the utility of these panels for CNV detection; (3) characterizing in detail the differences in CNV detection rates between individuals and lines; and (4) assessing the frequency of detected CNV and their possible functional impact. To achieve this, genes and quantitative trait loci (QTL) that overlap with the detected CNV were identified. Gene enrichment analysis was performed to identify overrepresented biological processes and pathways.
Samples and DNA extraction
Summary information for the SNP genotyping panels used
Number of genotyped individuals
Number of genotyped lines
Number of autosomal markers used
42K Illumina panel
50K Affymetrix panel for white layers
50K Affymetrix panel for brown layers
600K Affymetrix panel
SNP arrays and genotyping
SNP genotypes were obtained from several platforms over multiple years and for multiple purposes (Table 1).
The SNP panels used included the publicly available 600K Affymetrix chip , a 42K proprietary Illumina iSelecta BeadChip , and two custom 50K Affymetrix chips, which were designed separately for white and brown lines by HyLine International. The choice of SNPs for inclusion in each panel was based on their uniform distribution across the genome. The 42K Illumina panel was optimized to capture the genetic variance that is associated with economically important traits, and thus contained more SNPs in close proximity of genes than the other panels. For both 50K panels, only SNPs with high-quality clusters according to the Axiom™ Analysis Suite were included. This could have led to the elimination of SNPs that overlapped CNV in the birds used for panel design since those SNPs may not form three discrete clusters when plotting allele-A intensity versus allele-B intensity in Axiom™ Analysis Suite.
Detection of CNV
The Axiom™ Analysis Suite  was used to call genotypes for the 50K and 600K Affymetrix panels. A minimum default quality control of 0.82 and a minimum call rate of 97% were used. The Axiom® CNV Summary Tools software  was used to extract log R Ratio (LRR) and B allele frequency (BAF) values for PennCNV 1.0.3 . Genotype and CNV calling were performed separately for each 96-well genotyping plate because of the large differences in signal intensities between plates. Data from the 42K Illumina panel were processed in Genome Studio 2011.1 using the Genotyping module v 1.9 and the cnvPartition CNV Analysis Plugin v3.2.0 .
PennCNV, an integrated hidden Markov model (HMM), was used for all Affymetrix panels. This algorithm incorporates multiple sources of information, including the signal intensity data of LRR and BAF values at each SNP, the distance between neighboring SNPs, and the population frequency of the B allele (PFB). Individual-based CNV calling was performed using the—test option with default parameters for the HMM model. The hhall.hmm file was used with the—test option for all panels. To adjust for genomic waves, the—gcmodel option with the chicken GC content file (GC content of 1-Mb genomic regions surrounding each SNP) was used. The PFB files were compiled separately for each panel from a large set of individuals, using the compile pfb script included in the PennCNV software. For filtering, standard deviations (SD) for LRR ≤ 0.35, BAF drift < 0.01, and waviness factor ≤ 0.04 were used. The waviness factor accounts for the dispersion in signal intensity across the genome. Only CNV that consisted of at least three (for the 50K and 42K panels) or at least five (for the 600K panel) consecutive SNPs were included in the analysis. Individuals with more than 30 called CNV were excluded as unreliable (58 on the 600K, 47 on the 50K brown, 7 on the 50K white and 33 on the 42K panels). This number (30) was chosen as approximation of the mean number of CNV per individual plus 3 standard deviations across all panels. CNV were identified on autosomes (1 to 28) only because PennCNV calls for the sex chromosomes were unreliable and difficult to interpret.
Determination of CNV regions
For the list of all detected CNVR, a Bedtools merge was performed across all individuals and lines for all CNV that overlapped by at least 1 bp. This set is referred to as the merged CNVR.
Bedtools merge was performed for variants that were present in at least two individuals within a line. This set is referred to as the common CNVR.
Bedtools intersect was used for all CNV for a given panel and line combination, which were then merged across panels and lines. CNVR that were identified in at least two individuals within a line, were selected for further analysis. This set is referred to as common intersected CNVR.
CNVR that were detected in only one individual are referred to as singletons. CNVR for which both deletions and duplications were observed are referred to as complex CNVR.
Annotation of CNVR and gene ontology analysis
Genes that overlapped with common intersected CNVR were identified with the Ensembl BioMart webtool based on the Galgal4 assembly and the Ensembl Genes 85 database . Analysis of overrepresented GO terms and pathways was performed using PANTHER Classification System version 11 . Known quantitative trait loci (QTL) that overlapped with the detected CNVR were identified based on the Animal QTL database  release 33. In order to perform a comparison with previous studies, autosomal coordinates of the CNVR were migrated from galGal3 to galGal4 using the UCSC liftOver tool . Common CNV were checked visually using available sequence data, which consisted of representative pools of 10 individuals per line. Details on the sequencing of these pools are in Kranis et al. .
Detection of CNV
Summary of CNV identified for each line and each genotyping panel
Number of individuals
Number of individuals that pass quality control
Total number of CNVb
Mean N of CNV per individual
Mean length (kb)
Length range (kb)
The length of the CNV ranged from 1.2 kb to 3.2 Mb (Table 2). CNV shorter than 1 kb and that included less than 3, 3 or 5 SNPs for the 42K, 50K and 600K panels, respectively, were excluded from analysis. The mean length of detected CNV was greater for the 50K panels, which most likely resulted from the low detectability of shorter variants due to the greater distance between SNPs compared to the 600K panel. The length of each CNV was calculated as the distance from the first to the last SNP included in the CNV region, which may, therefore, slightly underestimate the true length.
Summary of CNVR detected for each line and genotyping panel
Number of CNVR
Number of deletions
Number of duplications
Number of complex CNVRc
Number of CNVR with a frequency > 1%d (maximum)
N ≥ 2b
N ≥ 2b
CNVR and overlapping genes
Summary of CNVR per chromosome for all panels
Chr length (Mb)
Merged CNVR N ≥ 2b
Intersected CNVR N ≥ 2c
Fraction of chr coveredd
Fraction of chr coveredd
In total, 2687 CNVR were identified after merging CNV across all samples and lines (Additional file 2: Table S2). The total length of these CNV was equal to 493.3 Mb, which corresponds to 53.7% of the analyzed genome sequence. Of the merged CNVR, 73.4% overlapped with genes, which accounted for 45.9% of the total CNVR sequence.
The number of common CNVR, which resulted from merging CNV that were found to be shared by at least two individuals within a line, was equal to 1264, with a total length of 375.8 Mb. Of these CNVR, 82.0% overlapped with genes, which encompassed 46.2% of the total CNVR sequence. More than 97.2% of the merged CNVR and 96.8% of the common CNVR overlapped with known QTL. Of the 1264 CNVR, 447 CNVR that cover 252.8 Mb, were detected by more than one SNP panel.
Gene ontology (GO) overrepresented terms for common CNVR (N = 2139)
PANTHER GO-Slim biological process
Antigen processing and presentation
B cell mediated immunity
Fatty acid biosynthetic process
Cellular defense response
Synaptic vesicle exocytosis
Within-line CNV characterization
Number of CNVR that overlapped between lines (above diagonal)
To determine whether CNV are associated with specific biological processes, we identified the genes within CNVR that were detected in at least two individuals within a line. In total, 682 genes overlapped with 465 merged CNVR for the 600K panel and 602 of these were mapped by Panther with 257 CNVR not classified in any GO term. Two terms were significant after Bonferroni correction, phagocytosis (p-value = 0.0250) and cellular defense response (p-value = 0.0127), with enrichments of 5.71 and 3.25, respectively.
Then, we performed the Panther GO overrepresentation test for genes that were identified within each line separately. No significant GO terms were identified for line W1, probably because of the small number of genotyped individuals and the small number of detected CNVR. For all the other lines, we detected several significant GO terms, but these were mostly connected to genes that overlapped with a single CNVR. For the hybrid cross, the most significant GO terms were: antigen processing and presentation, phagocytosis, B cell immunity, and cellular defense response. The antigen processing and presentation term was connected to CNVR that were identified on chromosome 16, which consisted of 13 CNV that covered almost the entire chromosome. The B cell immunity and cellular defense response terms, which were significant for lines B1, W2, and the hybrid cross, were connected to a region on chromosome 27, where a single copy deletion was observed between 0.19 and 0.33 Mb (Table 2).
Confirmation of CNVR with frequencies higher than 5%
In this study, we used 17,706 individuals from four pure lines and one commercial multi-line cross to detect CNV using genotypes provided by four SNP panels with different densities. In total, 19,525 CNV were detected, which resulted in 2687 CNVR after merging across individuals, lines, and panels. This result shows that CNV detection is possible by using commercially available SNP genotyping platforms. In addition, 19 high frequency CNVR were detected using the 600K panel, of which 57.9% overlapped with annotated genes (Additional file 1). We hypothesize that the CNV, which segregate within the lines at relatively high frequencies, may have an impact on the traits that are under selection in these lines.
CNV detection and comparison of results between SNP panels
Similar to other studies on the detection of CNV, duplications were more abundant than deletions [22, 30], although there were some differences between lines. For line B2, the number of losses was almost equal to the number of gains, which may be specific of this line or of the 42K panel, which was initially developed to exclude SNPs that did not perform well (thus some SNPs within CNV may have been eliminated). For line B1, the 600K panel, the number of losses was almost six times larger than the number of gains when the 600K panel was used, whereas interestingly, when the 50K panel was used, we obtained the opposite result, although most of the gains were due to singletons. These results may be due to the large difference in the number of line B1 individuals genotyped for these two panels, the low detectability with the 50K panel, and the large number of singletons.
Based on the literature, generally most of the detected CNV have low population frequencies, although the use of relatively small numbers of individuals can result in sampling bias. According to Jia et al. , among the 315 CNV that they detected in an analysis of 746 chickens with the 60K SNP array, only four had a frequency higher than 5% and none had a frequency higher than 10%. In addition, more recent studies have reported that most of the detected CNVR are singletons (occurring only in one individual), i.e. 76% in Han et al. , 69% in Yi et al. , and 75% in Strillacci et al. . In our study, we detected several common CNVR with a frequency higher than 5%, although most of these were detected only with the 600K panel (Table 2). The lower frequency of the CNVR detected when using the 50K and 42K panels confirm the advantage of higher SNP densities for CNV detection as previously reported [28, 30, 31].
Among all the detected CNVR, 46% were observed in a single individual across all lines. This observation, combined with the large number of individuals used in this study, confirms previous observations that a large fraction of CNV are singletons. However, such a large number of singletons could also result from the stringent quality control criteria that were applied in this study, including plate-by-plate detection, which could result in some CNV being overlooked.
The stringent quality control criteria that were applied when selecting SNPs for the 50K panel may have excluded SNPs in CNV regions. This hypothesis is supported by the larger number of CNV per individual, which were detected for the white layer line W1 when using the 50K panel that was developed specifically for brown layers compared to the 50K panel that was developed specifically for white layers (Table 1).
To summarize, although all panels enable the detection of CNV, it is possible that a proportion of the CNV that could be detected by more accurate data such as sequence data are missed when using SNP panels, especially lower density panels. In addition, a number of characteristics should be taken into account when calling CNV with SNP panels. First, distance between SNPs on the panel and their coverage have a clear effect on the length of the detected CNV. Second, it is necessary to have genotypes for a relatively large number of individuals to detect CNVR that are segregating within populations and to estimate their frequency. The pre-selection strategy for the SNPs placed on the panel also needs to be taken into account, since the SNPs that are located within CNV are more likely to be excluded as non-performing. Finally, the panel used can influence the ratio of detected deletions to duplications. In light of these results, our recommendation is that CNV detection using SNP genotypes can be used on a larger scale for commercial populations with large sample sizes, but keeping in mind the limitations.
Chromosome coverage and gene content
The number of CNV detected varied between chromosomes, with the microchromosomes being characterized by a higher density of CNV. In general, microchromosomes are known to have a higher gene content, which directly contradicts the observation that the majority of CNV are in gene-poor regions and gene deserts . Our results suggest the opposite, i.e. that microchromosomes are more CNV-rich than macrochromosomes and thus more frequently associated with genes, which is consistent with the findings of Skinner et al. . One of the most interesting cases is chromosome 16, which was covered at 98% by CNV, these being present in 53 individuals across all lines. This confirms a number of previous studies [28, 30]. The reason for this high density of CNV on chromosome 16 could be that it carries the major histocompatibility complex and has a high recombination rate, but the poor reference genome sequence for this chromosome could also be a cause. Details on the recombination rate and CNV located on chromosome 16 are in Fulton et al. .
Rao et al.  reported that only 38% of the 383 CNVR that they identified in chickens overlapped with genes. We observed a similarly small percentage (30%) for the 2139 intersected CNVR, which is probably related to the relatively short length of the intersected variants that fall within intergenic regions. These results support the hypothesis that a majority of CNVR is associated with genes and may have functional effects. In contrast, in a study on 16 bird species, Skinner et al.  determined that 70% of the detected CNVR overlapped with genes. We obtained a similar result for merged CNV, of which 73.4% overlapped with genes, and this percentage was even higher for the 1264 common CNVR (82.0%). These results support the hypothesis that the majority of CNVR is associated with genes and may have functional effects. In addition, GO analysis showed that genes that overlapped with CNV were enriched with a number of biological functions, in particular related to immune response. This is consistent with the results of Jia et al.  who suggested that this type of polymorphism might be prevalent in immune-related genes.
Comparison of CNVR detected in our work with previous studies
Additional file 5: Table S4 includes the list of the CNVR that were detected in this study and that overlap with previously detected CNVR. Of the 2687 CNVR that we detected, 70% overlapped with previously detected CNV, but these only comprise 28% of the total sequence length for all CNVR detected in this study. Of the 1264 common CNVR, 169 were novel and covered 2.4% of their total sequence (375.8 Mb). The total sequence overlap of common CNVR with previously known CNVR was equal to 32.6%, which can be related to the large length of merged CNVR. For both all and common CNVR, the sequence coverage with previously detected CNVR was around 30%. This observation, combined with the large number of singletons, leads to the conclusion that the occurrence of CNV is specific for each individual and inter-individual differences are more pronounced than between-line differences.
Summary of CNV detected in the chicken genome based on the 600K panel in the current and previous studies
Overall, we found a larger total number of CNV and a higher proportion of the genome covered by these CNV than previous studies in chickens [28, 30–32]. These differences are likely due to the much larger number of individuals analyzed in this study (Table 7), which allowed a better characterization of within-line CNV variability.
Of the 19 CNVR that were identified (based on the 600K panel) with a frequency of at least 5% within one line, 11 overlapped with at least one gene and 17 overlapped with a previously detected QTL (Additional file 6: Table S5). Among the QTL that overlapped with these common CNVR, 26 were involved in body weight and 13 in growth. The largest numbers of overlapping QTL were found for CNVR on chromosomes 2, 3, 4 and 5. The deletion on chromosome 8 overlapped with the largest number of genes (14) and with one QTL, for body weight. The GO terms that were enriched for the 600K CNV were mostly related to immune-response genes. This observation, along with the large number of singleton CNV identified, suggests a large inter-individual variability among the genes involved in immune response.
The high-frequency CNVR located at 179 Mb on chromosome 1 overlapped with a number of QTL for body weight and Marek’s disease related traits, and with the ALKBH8 gene. Wang et al.  had already reported this CNVR on chromosome 1 between 184,874,498 and 184,879,098 bp in build 3 of the chicken genome and predicted 45 candidate transcription factor binding sites for this region by WWW PROMOTER SCAN. This suggests that amplification of this upstream locus might affect expression of the ALKBH8 gene, which codes for tRNA methyltransferase and is involved in tRNA modifications and regulation of gene expression.
The second interesting high-frequency CNVR is a single copy deletion on chromosome 6 (12.47–12.54 Mb). This deletion does not overlap with a gene but it is located in close proximity to a number of genes, downstream to ZMIZ1 and upstream to RPS24 and POLR3A, which are all involved in immune response. This region also overlaps with 10 QTL, including one for antibody response to sheep red blood cells (SRBC).
The high-frequency CNVR deletion on chromosome 23 (between 2.34 and 2.35 Mb) overlaps with the gene RHCE (Rh blood group CcEe antigens). Previously detected QTL located within this region are involved in body weight and shank length. A duplication on chromosome 2 between 129.10 and 129.17 Mb overlaps with two genes, BAALC and FZD6, which are both connected to immune response. A CNV that overlaps with the FZD6 gene was previously reported by Yan et al.  and was associated with Marek’s disease resistance. This CNV also overlaps with two QTL in the Animal QTL database that are related to Marek’s disease and with cloacal bacterial burden following challenge with Salmonella.
Our results support previous findings that a large proportion of all detected CNVR are singletons, but we were able to detect several common CNVR, which may have important functional impacts. In addition, the large number of CNV that overlap with genes suggests that chicken CNV can impact agricultural or disease-related traits. In this context, the detection of structural variants such as CNV in chicken should be performed on a wider scale. The use of SNP genotypes on a large number of individuals enabled a better characterization of the CNV, both within and between lines. The list of CNVR presented here provides an additional resource for further studies in chicken. We observed pronounced differences between SNP panels and a clear advantage for the dense 600K SNP panel, both regarding the total number of CNV detected and their population frequencies. Although the use of SNP panels does not allow all the CNV that are present in an individual to be detected, these results show that they are a valuable source of CNV information by allowing the screening of large numbers of individuals at relatively low cost.
WDC conceived the study, performed the analysis and wrote the draft. AW contributed to the analysis, methods and discussion. JF collected the data and contributed to the discussion. JCMD contributed to the methods and discussion. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Availability of data and materials
The data that support the findings of this study are available from Hy-Line International but restrictions apply to the availability of these data, which were used under license for the current study, and thus are not publicly available. However, data are available from the authors upon reasonable request and with permission of Hy-Line International.
The data and the blood samples were collected on experimental farms that complied with the UEP (United Egg Producers) certified program for animal well-being.
Consent for publication
The study was supported by Warsaw University of Life Sciences travel fund and funding from Hy-Line International.
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