How structural variants shape avian phenotypes: Lessons from model systems.

Avian model systems chromosomal rearrangements genotype/phenotype associations pangenomes structural variants

Journal

Molecular ecology

ISSN: 1365-294X

Titre abrégé: Mol Ecol

Pays: England

ID NLM: 9214478

Informations de publication

Date de publication:
23 Apr 2024

Historique:

revised: 04 04 2024

received: 06 11 2023

accepted: 09 04 2024

medline: 23 4 2024

pubmed: 23 4 2024

entrez: 23 4 2024

Statut: aheadofprint

Résumé

Despite receiving significant recent attention, the relevance of structural variation (SV) in driving phenotypic diversity remains understudied, although recent advances in long-read sequencing, bioinformatics and pangenomic approaches have enhanced SV detection. We review the role of SVs in shaping phenotypes in avian model systems, and identify some general patterns in SV type, length and their associated traits. We found that most of the avian SVs so far identified are short indels in chickens, which are frequently associated with changes in body weight and plumage colouration. Overall, we found that relatively short SVs are more frequently detected, likely due to a combination of their prevalence compared to large SVs, and a detection bias, stemming primarily from the widespread use of short-read sequencing and associated analytical methods. SVs most commonly involve non-coding regions, especially introns, and when patterns of inheritance were reported, SVs associated primarily with dominant discrete traits. We summarise several examples of phenotypic convergence across different species, mediated by different SVs in the same or different genes and different types of changes in the same gene that can lead to various phenotypes. Complex rearrangements and supergenes, which can simultaneously affect and link several genes, tend to have pleiotropic phenotypic effects. Additionally, SVs commonly co-occur with single-nucleotide polymorphisms, highlighting the need to consider all types of genetic changes to understand the basis of phenotypic traits. We end by summarising expectations for when long-read technologies become commonly implemented in non-model birds, likely leading to an increase in SV discovery and characterisation. The growing interest in this subject suggests an increase in our understanding of the phenotypic effects of SVs in upcoming years.

Identifiants

DOI: 10.1111/mec.17364 PMID: 38651830

pubmed: 38651830

doi: 10.1111/mec.17364

doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

Pagination

e17364

Subventions

Organisme : Division of Environmental Biology

ID : NSF-DEB-2232929

Informations de copyright

Références

Abe, H., Nagao, K., & Inoue‐Murayama, M. (2013). Short copy number variations potentially associated with tonic immobility responses in newly hatched chicks. PLoS One, 8(11), e80205.

Adetula, A. A., Liu, X., Yang, L., Fang, C., Yu, H., Li, H., & Li, S. (2020). RAI14 in the blood feather regulates chicken pigmentation. Archives Animal Breeding, 63(2), 231–239.

Alonge, M., Wang, X., Benoit, M., Soyk, S., Pereira, L., Zhang, L., Suresh, H., Ramakrishnan, S., Maumus, F., Ciren, D., Levy, Y., Harel, T. H., Shalev‐Schlosser, G., Amsellem, Z., Razifard, H., Caicedo, A. L., Tieman, D. M., Klee, H., Kirsche, M., … Lippman, Z. B. (2020). Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell, 182(1), 145–161.e23.

Altgilbers, S., Dierks, C., Klein, S., Weigend, S., & Kues, W. A. (2022). Quantitative analysis of CRISPR/Cas9‐mediated provirus deletion in blue egg layer chicken PGCs by digital PCR. Scientific Reports, 12(1), 15587.

Bai, H., Sun, Y., Liu, N., Liu, Y., Xue, F., Li, Y., Xu, S., Ni, A., Ye, J., Chen, Y., & Chen, J. (2018). Genome‐wide detection of CNV s associated with beak deformity in chickens using high‐density 600K SNP arrays. Animal Genetics, 49(3), 226–236.

Bed'hom, B., Vaez, M., Coville, J. L., Gourichon, D., Chastel, O., Follett, S., Bruke, T., & Minvielle, F. (2012). The lavender plumage colour in Japanese quail is associated with a complex mutation in the region of MLPH that is related to differences in growth, feed consumption and body temperature. BMC Genomics, 13, 1–10.

Belton, J. M., McCord, R. P., Gibcus, J. H., Naumova, N., Zhan, Y., & Dekker, J. (2012). Hi–C: A comprehensive technique to capture the conformation of genomes. Methods, 58(3), 268–276.

Bickhart, D. M., & Liu, G. E. (2014). The challenges and importance of structural variation detection in livestock. Frontiers in Genetics, 5, 37.

Boman, J., Frankl‐Vilches, C., da Silva dos Santos, M., de Oliveira, E. H., Gahr, M., & Suh, A. (2019). The genome of blue‐capped cordon‐bleu uncovers hidden diversity of LTR retrotransposons in zebra finch. Genes, 10(4), 301.

Bourgeois, Y., & Boissinot, S. (2019). On the population dynamics of junk: A review on the population genomics of transposable elements. Genes, 10(6), 419.

Bourque, G., Burns, K. H., Gehring, M., Gorbunova, V., Seluanov, A., Hammell, M., Imbeault, M., Izsvák, Z., Levin, H. L., Macfarlan, T. S., Mager, D. L., & Feschotte, C. (2018). Ten things you should know about transposable elements. Genome Biology, 19, 1–12.

Broman, K. W. (2001). Review of statistical methods for QTL mapping in experimental crosses. Lab Animal, 30(7), 44–52.

Bruders, R., Van Hollebeke, H., Osborne, E. J., Kronenberg, Z., Maclary, E., Yandell, M., & Shapiro, M. D. (2020). A copy number variant is associated with a spectrum of pigmentation patterns in the rock pigeon (Columba livia). PLoS Genetics, 16(5), e1008274.

Caballero‐López, V., Lundberg, M., Sokolovskis, K., & Bensch, S. (2022). Transposable elements mark a repeat‐rich region associated with migratory phenotypes of willow warblers (Phylloscopus trochilus). Molecular Ecology, 31(4), 1128–1141.

Campagna, L., & Toews, D. P. (2022). The genomics of adaptation in birds. Current Biology, 32(20), R1173–R1186.

Chang, C. F., Schock, E. N., O'Hare, E. A., Dodgson, J., Cheng, H. H., Muir, W. M., Edelmann, R. E., Delany, M. E., & Brugmann, S. A. (2014). The cellular and molecular etiology of the craniofacial defects in the avian ciliopathic mutant talpid2. Development, 141(15), 3003–3012.

Chang, C. M., Coville, J. L., Coquerelle, G., Gourichon, D., Oulmouden, A., & Tixier‐Boichard, M. (2006). Complete association between a retroviral insertion in the tyrosinase gene and the recessive white mutation in chickens. BMC Genomics, 7, 1–15.

Chen, B., Xi, S., el‐Senousey, H. K., Zhou, M., Cheng, D., Chen, K., Wan, L., Xiong, T., Liao, M., Liu, S., & Mao, H. (2022). Deletion in KRT75L4 linked to frizzle feather in Xiushui yellow chickens. Animal Genetics, 53(1), 101–107.

Chen, X., Bai, X., Liu, H., Zhao, B., Yan, Z., Hou, Y., & Chu, Q. (2022). Population genomic sequencing delineates global landscape of copy number variations that drive domestication and breed formation of in chicken. Frontiers in Genetics, 13, 830393.

Chiang, C., Scott, A. J., Davis, J. R., Tsang, E. K., Li, X., Kim, Y., Hadzic, T., Damani, F. N., Ganel, L., GTEx Consortium, Montgomery, S. B., Battle, A., Conrad, D. F., & Hall, I. M. (2017). The impact of structural variation on human gene expression. Nature Genetics, 49(5), 692–699.

Cui, J. X., Du, H. L., Liang, Y., Deng, X. M., Li, N., & Zhang, X. Q. (2006). Association of polymorphisms in the promoter region of chicken prolactin with egg production. Poultry Science, 85(1), 26–31.

Delmore, K. E., Van Doren, B. M., Ullrich, K., Curk, T., van der Jeugd, H. P., & Liedvogel, M. (2023). Structural genomic variation and migratory behavior in a wild songbird. Evolution Letters, 7(6), 401–412. https://doi.org/10.1093/evlett/qrad040

Derks, M. F., Herrero‐Medrano, J. M., Crooijmans, R. P., Vereijken, A., Long, J. A., Megens, H. J., & Groenen, M. A. (2018). Early and late feathering in Turkey and chicken: Same gene but different mutations. Genetics Selection Evolution, 50(1), 1–7.

Domyan, E. T., Guernsey, M. W., Kronenberg, Z., Krishnan, S., Boissy, R. E., Vickrey, A. I., Rodgers, C., Cassidy, P., Leachman, S. A., Fondon, J. W., III, Yandell, M., & Shapiro, M. D. (2014). Epistatic and combinatorial effects of pigmentary gene mutations in the domestic pigeon. Current Biology, 24(4), 459–464.

Domyan, E. T., Kronenberg, Z., Infante, C. R., Vickrey, A. I., Stringham, S. A., Bruders, R., Guernsey, M. W., Park, S., Payne, J., Beckstead, R. B., Kardon, G., Menke, D. B., Yandell, M., & Shapiro, M. D. (2016). Molecular shifts in limb identity underlie development of feathered feet in two domestic avian species. eLife, 5, e12115.

Dong, J., He, C., Wang, Z., Li, Y., Li, S., Tao, L., Chen, J., Li, D., Yang, F., Li, N., Zhang, Q., Zhang, L., Wang, G., Akinyemi, F., Meng, H., & Du, B. (2018). A novel deletion in KRT75L4 mediates the frizzle trait in a Chinese indigenous chicken. Genetics Selection Evolution, 50(1), 1–9.

Dorshorst, B., Harun‐Or‐Rashid, M., Bagherpoor, A. J., Rubin, C. J., Ashwell, C., Gourichon, D., Tixier‐Boichard, M., Hallböök, F., & Andersson, L. (2015). A genomic duplication is associated with ectopic eomesodermin expression in the embryonic chicken comb and two duplex‐comb phenotypes. PLoS Genetics, 11(3), e1004947.

Dorshorst, B., Molin, A. M., Rubin, C. J., Johansson, A. M., Strömstedt, L., Pham, M. H., Chen, C. F., Hallböök, F., Ashwell, C., & Andersson, L. (2011). A complex genomic rearrangement involving the endothelin 3 locus causes dermal hyperpigmentation in the chicken. PLoS Genetics, 7(12), e1002412.

Drobik‐Czwarno, W., Wolc, A., Fulton, J. E., & Dekkers, J. C. (2018). Detection of copy number variations in brown and white layers based on genotyping panels with different densities. Genetics Selection Evolution, 50, 1–13.

Elferink, M. G., Vallée, A. A., Jungerius, A. P., Crooijmans, R. P., & Groenen, M. A. (2008). Partial duplication of the PRLR and SPEF2 genes at the late feathering locus in chicken. BMC Genomics, 9(1), 1–9.

Fagny, M., & Austerlitz, F. (2021). Polygenic adaptation: Integrating population genetics and gene regulatory networks. Trends in Genetics, 37(7), 631–638.

Falker‐Gieske, C., Bennewitz, J., & Tetens, J. (2023). Structural variation and eQTL analysis in two experimental populations of chickens divergently selected for feather‐pecking behavior. Neurogenetics, 24(1), 29–41.

Fan, W. L., Ng, C. S., Chen, C. F., Lu, M. Y. J., Chen, Y. H., Liu, C. J., Wu, S. M., Chen, C. K., Chen, J. J., Mao, C. T., Lai, Y. T., Lo, W. S., Chang, W. H., & Li, W. H. (2013). Genome‐wide patterns of genetic variation in two domestic chickens. Genome Biology and Evolution, 5(7), 1376–1392.

Fernandes, A. C., da Silva, V. H., Goes, C. P., Moreira, G. C. M., Godoy, T. F., Ibelli, A. M. G., Peixoto, J. O., Cantão, M. E., Ledur, M. C., de Rezende, F. M., & Coutinho, L. L. (2021). Genome‐wide detection of CNVs and their association with performance traits in broilers. BMC Genomics, 22(1), 1–18.

Fu, R., Ren, T., Li, W., Liang, J., Mo, G., Luo, W., He, D., Liang, S., & Zhang, X. (2020). A novel 65‐bp Indel in the GOLGB1 gene is associated with chicken growth and carcass traits. Animals, 10(3), 475.

Geibel, J., Praefke, N. P., Weigend, S., Simianer, H., & Reimer, C. (2022). Assessment of linkage disequilibrium patterns between structural variants and single nucleotide polymorphisms in three commercial chicken populations. BMC Genomics, 23(1), 193.

Gong, Y., Li, Y., Liu, X., Ma, Y., & Jiang, L. (2023). A review of the pangenome: How it affects our understanding of genomic variation, selection and breeding in domestic animals? Journal of Animal Science and Biotechnology, 14(1), 1–19.

Gu, L., Sun, C., Gong, Y., Yu, M., & Li, S. (2017). Novel copy number variation of the TGFβ3 gene is associated with TGFβ3 gene expression and duration of fertility traits in hens. PLoS One, 12(3), e0173696.

Gunnarsson, U., Kerje, S., Bed'hom, B., Sahlqvist, A. S., Ekwall, O., Tixier‐Boichard, M., Kämpe, O., & Andersson, L. (2011). The dark brown plumage color in chickens is caused by an 8.3‐kb deletion upstream of SOX10. Pigment Cell & Melanoma Research, 24(2), 268–274.

Guo, Y., Gu, X., Sheng, Z., Wang, Y., Luo, C., Liu, R., Qu, H., Shu, D., Wen, J., Crooijmans, R. P., Carlborg, Ö., Zhao, Y., Hu, X., & Li, N. (2016). A complex structural variation on chromosome 27 leads to the ectopic expression of HOXB8 and the muffs and beard phenotype in chickens. PLoS Genetics, 12(6), e1006071.

Han, R., Wang, X., Wang, X., Guo, Y., Li, D., Li, G., Wang, Y., Kang, X., & Li, Z. (2019). Chicken ZNF764L gene: mRNA expression profile, alternative splicing analysis and association analysis between first exon indel mutation and economic traits. Gene, 695, 92–98.

Han, R., Yang, P., Tian, Y., Wang, D., Zhang, Z., Wang, L., Li, Z., Jiang, R., & Kang, X. (2014). Identification and functional characterization of copy number variations in diverse chicken breeds. BMC Genomics, 15(1), 1–10.

Han, R. L., Li, Z. J., Li, M. J., Li, J. Q., Lan, X. Y., Sun, G. R., Kang, X. T., & Chen, H. (2011). Novel 9‐bp indel in visfatin gene and its associations with chicken growth. British Poultry Science, 52(1), 52–57.

He, J., Fu, T., Zhang, L., Gao, L. W., Rensel, M., Remage‐Healey, L., White, S. A., Gedman, G., Whitelegge, J., Xiao, X., & Schlinger, B. A. (2022). Improved zebra finch brain transcriptome identifies novel proteins with sex differences. Gene, 843, 146803.

He, K., Minias, P., & Dunn, P. O. (2021). Long‐read genome assemblies reveal extraordinary variation in the number and structure of MHC loci in birds. Genome Biology and Evolution, 13(2), evaa270.

Hiragaki, T., Inoue‐Murayama, M., Miwa, M., Fujiwara, A., Mizutani, M., Minvielle, F., & Ito, S. I. (2008). Recessive black is allelic to the yellow plumage locus in Japanese quail and associated with a frameshift deletion in the ASIP gene. Genetics, 178(2), 771–775.

Hirwa, C. D. A., Yan, W., Wallace, P., Nie, Q., Luo, C., Li, H., Shen, X., Sun, L., Tang, J., Li, W., Zhu, X., Yang, G., & Zhang, X. (2010). Effects of the thyroid hormone responsive spot 14α gene on chicken growth and fat traits. Poultry Science, 89(9), 1981–1991.

Huang, T., Cheng, S., Feng, Y., Sheng, Z., & Gong, Y. (2018). A copy number variation generated by complicated organization of PCDHA gene cluster is associated with egg performance traits in Xinhua E‐strain. Poultry Science, 97(10), 3435–3445.

Huang, Y., Boskovic, G., & Niles, R. M. (2003). Retinoic acid‐induced AP‐1 transcriptional activity regulates B16 mouse melanoma growth inhibition and differentiation. Journal of Cellular Physiology, 194(2), 162–170.

Imsland, F., Feng, C., Boije, H., Bed'hom, B., Fillon, V., Dorshorst, B., Rubin, C. J., Liu, R., Gao, Y., Gu, X., Wang, Y., Gourichon, D., Zody, M. C., Zecchin, W., Vieaud, A., Tixier‐Boichard, M., Hu, X., Hallböök, F., Li, N., & Andersson, L. (2012). The rose‐comb mutation in chickens constitutes a structural rearrangement causing both altered comb morphology and defective sperm motility. PLoS Genetics, 8(6), e1002775.

Jin, S., Zhu, F., Wang, Y., Yi, G., Li, J., Lian, L., Zheng, J., Xu, G., Jiao, R., Gong, Y., Hou, Z., & Yang, N. (2016). Deletion of Indian hedgehog gene causes dominant semi‐lethal creeper trait in chicken. Scientific Reports, 6(1), 30172.

Jing, Z., Wang, X., Cheng, Y., Wei, C., Hou, D., Li, T., Li, W., Han, R., Li, H., Sun, G., Tian, Y., Liu, X., Kang, X., & Li, Z. (2020). Detection of CNV in the SH3RF2 gene and its effects on growth and carcass traits in chickens. BMC Genetics, 21(1), 1–7.

Kapusta, A., & Suh, A. (2017). Evolution of bird genomes—A transposon's‐eye view. Annals of the New York Academy of Sciences, 1389(1), 164–185.

Khatri, B., Kang, S., Shouse, S., Anthony, N., Kuenzel, W., & Kong, B. C. (2019). Copy number variation study in Japanese quail associated with stress related traits using whole genome re‐sequencing data. PLoS One, 14(3), e0214543.

Kim, K. W., Bennison, C., Hemmings, N., Brookes, L., Hurley, L. L., Griffith, S. C., Burke, T., Birkhead, T. R., & Slate, J. (2017). A sex‐linked supergene controls sperm morphology and swimming speed in a songbird. Nature Ecology & Evolution, 1(8), 1168–1176.

Kinoshita, K., Suzuki, T., Koike, M., Nishida, C., Koike, A., Nunome, M., Uemura, T., Ichiyanagi, K., & Matsuda, Y. (2020). Combined deletions of IHH and NHEJ1 cause chondrodystrophy and embryonic lethality in the creeper chicken. Communications Biology, 3(1), 144.

Knief, U., Bossu, C. M., Saino, N., Hansson, B., Poelstra, J., Vijay, N., Weissensteiner, M., & Wolf, J. B. W. (2019). Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone. Nature Ecology & Evolution, 3(4), 570–576.

Knief, U., Forstmeier, W., Pei, Y., Ihle, M., Wang, D., Martin, K., Opatová, P., Albrechtová, J., Wittig, M., Franke, A., Albrecht, T., & Kempenaers, B. (2017). A sex‐chromosome inversion causes strong overdominance for sperm traits that affect siring success. Nature Ecology & Evolution, 1(8), 1177–1184.

Knief, U., Hemmrich‐Stanisak, G., Wittig, M., Franke, A., Griffith, S. C., Kempenaers, B., & Forstmeier, W. (2016). Fitness consequences of polymorphic inversions in the zebra finch genome. Genome Biology, 17(1), 1–22.

Komiyama, T., Iwama, H., Osada, N., Nakamura, Y., Kobayashi, H., Tateno, Y., & Gojobori, T. (2014). Dopamine receptor genes and evolutionary differentiation in the domestication of fighting cocks and long‐crowing chickens. PLoS One, 9(7), e101778.

Krause, E. T., Kjaer, J. B., Dudde, A., Schrader, L., & Phi‐van, L. (2019). Fear but not social behaviour is affected by a polymorphism in the 5′‐flanking region of the serotonin transporter (5‐HTT) gene in adult hens. Behavioural Brain Research, 361, 50–53.

Krishnan, S. (2019). Nested tandem duplications of the gene melanoma antigen recognized by T‐cells (Mlana) underlie the sexual dimorphism locus in domestic pigeons. bioRxiv, 754986.

Krishnan, S., & Cryberg, R. L. (2019). Effects of mutations in pigeon Mc1r implicate an expanded plumage color patterning regulatory network. bioRxiv, 792945.

Küpper, C., Stocks, M., Risse, J. E., Dos Remedios, N., Farrell, L. L., McRae, S. B., Morgan, T. C., Karlionova, N., Pinchuk, P., Verkuil, Y. I., Kitaysky, A. S., Wingfield, J. C., Piersma, T., Zeng, K., Slate, J., Blaxter, M., Lank, D. B., & Burke, T. (2016). A supergene determines highly divergent male reproductive morphs in the ruff. Nature Genetics, 48(1), 79–83. https://doi.org/10.1038/ng.3443

Lan, L. T. T., Nhan, N. T. H., Hung, L. T., Soubra, R. L., Gia, T. T., Anh, L. H., & Ngu, N. T. (2021). Association of polymorphisms in prolactin receptor and melatonin receptor 1c genes on egg production and egg quality traits of Japanese quails (Coturnix coturnix japonica). JAPS, 31(6), 1559–1567.

Li, J., Lee, M., Davis, B. W., Lamichhaney, S., Dorshorst, B. J., Siegel, P. B., & Andersson, L. (2020). Mutations upstream of the TBX5 and PITX1 transcription factor genes are associated with feathered legs in the domestic chicken. Molecular Biology and Evolution, 37(9), 2477–2486.

Li, J., Lee, M. O., Davis, B. W., Wu, P., Hsieh Li, S. M., Chuong, C. M., & Andersson, L. (2021). The crest phenotype in domestic chicken is caused by a 195 bp duplication in the intron of HOXC10. G3, 11(2), jkaa048.

Li, N., He, Q., Wang, J., Wang, B., Zhao, J., Huang, S., Yang, T., Tang, Y., Yang, S., Aisimutuola, P., Xu, R., Hu, J., Jia, C., Ma, K., Li, Z., Jiang, F., Gao, J., Lan, H., Zhou, Y., … Yu, Q. (2023). Super‐pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nature Genetics, 55(5), 852–860.

Li, T., Chen, B., Wei, C., Hou, D., Qin, P., Jing, Z., Ma, H., Niu, X., Wang, C., Han, R., Li, H., Liu, X., Xu, H., Kang, X., & Li, Z. (2021). A 104‐bp structural variation of the ADPRHL1 gene is associated with growth traits in chickens. Frontiers in Genetics, 12, 691272.

Li, T., Qin, P., Chen, B., Niu, X., Wang, Y., Niu, Y., Wei, C., Hou, D., Ma, H., Han, R., Li, H., Liu, X., Kang, X., & Li, Z. (2022). A novel 27‐bp indel in the intron region of the YBX3 gene is associated with growth traits in chickens. British Poultry Science, 63(5), 590–596.

Liao, W. W., Asri, M., Ebler, J., Doerr, D., Haukness, M., Hickey, G., Lu, S., Lucas, J. K., Monlong, J., Abel, H. J., Buonaiuto, S., Chang, X. H., Cheng, H., Chu, J., Colonna, V., Eizenga, J. M., Feng, X., Fischer, C., Fulton, R. S., … Paten, B. (2023). A draft human pangenome reference. Nature, 617(7960), 312–324.

Lin, W., Ren, T., Li, W., Liu, M., He, D., Liang, S., Luo, W., & Zhang, X. (2021). Novel 61‐bp indel of RIN2 is associated with fat and hatching weight traits in chickens. Frontiers in Genetics, 12, 672888.

Lin, Z. T., Chen, G. H., Peng, X., Zhang, Z. H., Li, T., Lin, H. X., Liang, S. S., Zheng, Y. B., Yao, Z. P., & Luo, W. (2023). A 2‐bp deletion in intron 1 of TMEM182 is associated with TMEM182 mRNA expression and chicken body weight. British Poultry Science, 64(1), 11–18.

Liu, X., Liu, L., Wang, J., Cui, H., Chu, H., Bi, H., Zhao, G., & Wen, J. (2020). Genome‐wide association study of muscle glycogen in jingxing yellow chicken. Genes, 11(5), 497.

Lundberg, M., Mackintosh, A., Petri, A., & Bensch, S. (2023). Inversions maintain differences between migratory phenotypes of a songbird. Nature Communications, 14(1), 452.

Luo, C., Shen, X., Rao, Y., Xu, H., Tang, J., Sun, L., Nie, Q., & Zhang, X. (2012). Differences of Z chromosome and genomic expression between early‐and late‐feathering chickens. Molecular Biology Reports, 39, 6283–6288.

Maclary, E. T., Wauer, R., Phillips, B., Brown, A., Boer, E. F., Samani, A. M., & Shapiro, M. (2023). An allelic series at the EDNRB2 locus controls diverse piebalding patterns in the domestic pigeon. bioRxiv, 2023‐07.

Mahmoud, M., Gobet, N., Cruz‐Dávalos, D. I., Mounier, N., Dessimoz, C., & Sedlazeck, F. J. (2019). Structural variant calling: The long and the short of it. Genome Biology, 20(1), 1–14.

Mahmoud, M., Huang, Y., Garimella, K., Audano, P. A., Wan, W., Prasad, N., Handsaker, R. E., Hall, S., Pionzio, A., Schatz, M. C., Talkowski, M. E., Eichler, E. E., Levy, S. E., & Sedlazeck, F. J. (2024). Utility of long‐read sequencing for all of us. Nature Communications, 15(1), 837.

Manoharan, A., Sankaralingam, S., Anitha, P., Chacko, B., & Aravindakshan, T. V. (2021). Identification of 24bp indel (s) polymorphism in the promoter region of prolactin gene and its association with broodiness in Tellicherry native chicken. Indian Journal of Animal Research, 55(10), 1137–1140.

Mérot, C., Oomen, R. A., Tigano, A., & Wellenreuther, M. (2020). A roadmap for understanding the evolutionary significance of structural genomic variation. Trends in Ecology & Evolution, 35(7), 561–572.

Minvielle, F., Bed'Hom, B., Coville, J. L., Ito, S. I., Inoue‐Murayama, M., & Gourichon, D. (2010). The" silver" Japanese quail and the MITF gene: Causal mutation, associated traits and homology with the" blue" chicken plumage. BMC Genetics, 11, 1–7.

Moro, C., Cornette, R., Vieaud, A., Bruneau, N., Gourichon, D., Bed'hom, B., & Tixier‐Boichard, M. (2015). Quantitative effect of a CNV on a morphological trait in chickens. PLoS One, 10(3), e0118706.

Mou, C., Pitel, F., Gourichon, D., Vignoles, F., Tzika, A., Tato, P., Yu, L., Burt, D. W., Bed'hom, B., Tixier‐Boichard, M., Painter, K. J., & Headon, D. J. (2011). Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering. PLoS Biology, 9(3), e1001028.

Ng, C. S., Wu, P., Foley, J., Foley, A., McDonald, M. L., Juan, W. T., Huang, C. J., Lai, Y. T., Lo, W. S., Chen, C. F., Leal, S. M., Zhang, H., Widelitz, R. B., Patel, P. I., Li, W. H., & Chuong, C. M. (2012). The chicken frizzle feather is due to an α‐keratin (KRT75) mutation that causes a defective rachis. PLoS Genetics, 8(7), e1002748.

Qin, P., Liu, Y., Niu, X., Liu, Y., Zhang, Y., Niu, Y., Wang, Y., Chen, B., Han, R., Tian, Y., Liu, X., Kang, X., Jiang, R., & Li, Z. (2023). Molecular characterization, expression profile, and a 21‐bp indel within the ASB9 gene and its associations with chicken production traits. Genes, 14(2), 339.

Rao, Y. S., Li, J., Zhang, R., Lin, X. R., Xu, J. G., Xie, L., Xu, Z. Q., Wang, L., Gan, J. K., Xie, X. J., He, J., & Zhang, X. Q. (2016). Copy number variation identification and analysis of the chicken genome using a 60K SNP BeadChip. Poultry Science, 95(8), 1750–1756.

Ren, T., Zhang, Z., Fu, R., Yang, Y., Li, W., Liang, J., Mo, G., Luo, W., & Zhang, X. (2020). A 51 bp indel polymorphism within the PTH1R gene is significantly associated with chicken growth and carcass traits. Animal Genetics, 51(4), 568–578.

Rice, E. S., Alberdi, A., Alfieri, J., Athrey, G., Balacco, J. R., Bardou, P., Blackmon, H., Charles, M., Cheng, H. H., Fedrigo, O., Fiddaman, S. R., Formenti, G., Frantz, L. A. F., Gilbert, M. T. P., Hearn, C. J., Jarvis, E. D., Klopp, C., Marcos, S., Mason, A. S., … Warren, W. C. (2023). A pangenome graph reference of 30 chicken genomes allows genotyping of large and complex structural variants. BMC Biology, 21, 267.

Robic, A., Morisson, M., Leroux, S., Gourichon, D., Vignal, A., Thebault, N., Fillon, V., Minvielle, F., Bed'Hom, B., Zerjal, T., & Pitel, F. (2019). Two new structural mutations in the 5′ region of the ASIP gene cause diluted feather color phenotypes in Japanese quail. Genetics Selection Evolution, 51(1), 1–10.

Rubin, C. J., Zody, M. C., Eriksson, J., Meadows, J. R., Sherwood, E., Webster, M. T., Jiang, L., Ingman, M., Sharpe, T., Ka, S., Hallböök, F., Besnier, F., Carlborg, O., Bed'hom, B., Tixier‐Boichard, M., Jensen, P., Siegel, P., Lindblad‐Toh, K., & Andersson, L. (2010). Whole‐genome resequencing reveals loci under selection during chicken domestication. Nature, 464(7288), 587–591.

Sacristán‐Horcajada, E., González‐de la Fuente, S., Peiró‐Pastor, R., Carrasco‐Ramiro, F., Amils, R., Requena, J. M., Berenguer, J. M., & Aguado, B. (2021). ARAMIS: From systematic errors of NGS long reads to accurate assemblies. Briefings in Bioinformatics, 22(6), bbab170.

Sanchez‐Donoso, I., Ravagni, S., Rodríguez‐Teijeiro, J. D., Christmas, M. J., Huang, Y., Maldonado‐Linares, A., Puigcerver, M., Jiménez‐Blasco, I., Andrade, P., Gonçalves, D., Friis, G., Roig, I., Webster, M. T., Leonard, J. A., & Vilà, C. (2022). Massive genome inversion drives coexistence of divergent morphs in common quails. Current Biology, 32(2), 462–469.e6.

Sato, S., Sato, S., Otake, T., Suzuki, C., Uemoto, Y., Saburi, J., Hashimoto, H., Hashimoto, H., & Kobayashi, E. (2010). Sequence analysis of a pea comb locus on chicken chromosome 1. Animal Genetics, 41(6), 659–661.

Secomandi, S., Gallo, G. R., Sozzoni, M., Iannucci, A., Galati, E., Abueg, L., Balacco, J., Caprioli, M., Chow, W., Ciofi, C., Collins, J., Fedrigo, O., Ferretti, L., Fungtammasan, A., Haase, B., Howe, K., Kwak, W., Lombardo, G., Masterson, P., … Formenti, G. (2023). A chromosome‐level reference genome and pangenome for barn swallow population genomics. Cell Reports, 42(1), 111992.

Seol, D., Ko, B. J., Kim, B., Chai, H. H., Lim, D., & Kim, H. (2019). Identification of copy number variation in domestic chicken using whole‐genome sequencing reveals evidence of selection in the genome. Animals, 9(10), 809.

Shen, Q., Li, J., Bao, H., & Wu, C. (2023). Identification of duplication genotypes of the feathering rate gene in chicken by a multiplex PCR following electrophoresis and/or sanger sequencing. Animals, 13(6), 1091.

Shen, Q., Zhou, J., Li, J., Zhao, X., Zheng, L., Bao, H., & Wu, C. (2022). Genome‐wide association study identifies candidate genes for stripe pattern feather color of Rhode Island red chicks. Genes, 13(9), 1511.

Shinomiya, A., Kayashima, Y., Kinoshita, K., Mizutani, M., Namikawa, T., Matsuda, Y., & Akiyama, T. (2012). Gene duplication of endothelin 3 is closely correlated with the hyperpigmentation of the internal organs (Fibromelanosis) in silky chickens. Genetics, 190(2), 627–638.

Singhal, S., Leffler, E. M., Sannareddy, K., Turner, I., Venn, O., Hooper, D. M., Strand, A. I., Li, Q., Raney, B., Balakrishnan, C. N., Griffith, S. C., McVean, G., & Przeworski, M. (2015). Stable recombination hotspots in birds. Science, 350(6263), 928–932.

Sohrabi, S. S., Mohammadabadi, M., Wu, D. D., & Esmailizadeh, A. (2018). Detection of breed‐specific copy number variations in domestic chicken genome. Genome, 61(1), 7–14.

Spielmann, M., Lupiáñez, D. G., & Mundlos, S. (2018). Structural variation in the 3D genome. Nature Reviews Genetics, 19(7), 453–467.

Strillacci, M. G., Gorla, E., Ríos‐Utrera, A., Vega‐Murillo, V. E., Montaño‐Bermudez, M., Garcia‐Ruiz, A., Cerolini, S., Román‐Ponce, S. I., & Bagnato, A. (2019). Copy number variation mapping and genomic variation of autochthonous and commercial Turkey populations. Frontiers in Genetics, 10, 982.

Strillacci, M. G., Marelli, S. P., Milanesi, R., Zaniboni, L., Punturiero, C., & Cerolini, S. (2021). Copy number variants in four Italian Turkey breeds. Animals, 11(2), 391.

Stuart, K. C., Edwards, R. J., Sherwin, W. B., & Rollins, L. A. (2023). Contrasting patterns of single nucleotide polymorphisms and structural variation across multiple invasions. Molecular Biology and Evolution, 40(3), msad046.

Suh, A., Smeds, L., & Ellegren, H. (2018). Abundant recent activity of retrovirus‐like retrotransposons within and among flycatcher species implies a rich source of structural variation in songbird genomes. Molecular Ecology, 27(1), 99–111.

Taylor, S., & Campagna, L. (2016). Avian supergenes. Science, 351(6272), 446–447.

Tuttle, E. M., Bergland, A. O., Korody, M. L., Brewer, M. S., Newhouse, D. J., Minx, P., Stager, M., Betuel, A., Cheviron, Z. A., Warren, W. C., Gonser, R. A., & Balakrishnan, C. N. (2016). Divergence and functional degradation of a sex chromosome‐like supergene. Current Biology, 26(3), 344–350.

Uffelmann, E., Huang, Q. Q., Munung, N. S., De Vries, J., Okada, Y., Martin, A. R., Martin, H. C., Lappalainen, T., & Posthuma, D. (2021). Genome‐wide association studies. Nature Reviews Methods Primers, 1(1), 59.

van Dijk, E. L., Naquin, D., Gorrichon, K., Jaszczyszyn, Y., Ouazahrou, R., Thermes, C., & Hernandez, C. (2023). Genomics in the long‐read sequencing era. Trends in Genetics, 39(9), 649–671.

Vickrey, A. I., Bruders, R., Kronenberg, Z., Mackey, E., Bohlender, R. J., Maclary, E. T., Maynez, R., Osborne, E. J., Johnson, K. P., Huff, C. D., Yandell, M., & Shapiro, M. D. (2018). Introgression of regulatory alleles and a missense coding mutation drive plumage pattern diversity in the rock pigeon. eLife, 7, e34803.

Vinh, N. T., Giang, N. T. P., Linh, N. V., Dang, P. K., Cahn, N. X., Giang, N. T. C., Doan, B. H., Anh, N. T., & Thinh, N. H. (2021). Single nucleotide polymorphisms of candidate genes related to egg production traits in Vietnamese indigenous chickens. Brazilian Journal of Poultry Science, 23, eRBCA‐2020‐1298.

Wang, J., Xi, Y., Ma, S., Qi, J., Li, J., Zhang, R., Han, C., Li, L., Wang, J., & Liu, H. (2022). Single‐molecule long‐read sequencing reveals the potential impact of posttranscriptional regulation on gene dosage effects on the avian Z chromosome. BMC Genomics, 23(1), 1–14.

Wang, K., Hu, H., Tian, Y., Li, J., Scheben, A., Zhang, C., Li, Y., Wu, J., Yang, L., Fan, X., Sun, G., Li, D., Zhang, Y., Han, R., Jiang, R., Huang, H., Yan, F., Wang, Y., Li, Z., … Kang, X. (2021). The chicken pan‐genome reveals gene content variation and a promoter region deletion in IGF2BP1 affecting body size. Molecular Biology and Evolution, 38(11), 5066–5081.

Wang, K., Hua, G., Li, J., Yang, Y., Zhang, C., Yang, L., Hu, X., Scheben, A., Wu, Y., Gong, P., Zhang, S., Fan, Y., Zeng, T., Lu, L., Gong, Y., Jiang, R., Sun, G., Tian, Y., Kang, X., … Li, W. (2023). Duck pan‐genome reveals two transposon‐derived structural variations caused bodyweight enlarging and white plumage phenotype formation during evolution. bioRxiv, 2023‐01.

Wang, X., Wang, X., Chen, B., Guo, Y., Tang, H., Li, D., Hu, X., Scheben, A., Wu, Y., Gong, P., Zhang, S., Fan, Y., Zeng, T., Lu, L., Gong, Y., Jiang, R., Sun, G., Tian, Y., Kang, X., … Han, R. (2020). Association of a new 99‐bp indel of the CEL gene promoter region with phenotypic traits in chickens. Scientific Reports, 10(1), 3215.

Wang, X., Wei, C., Zhang, Z., Liu, D., Guo, Y., Sun, G., Wang, Y., Li, H., Tian, Y., Kang, X., Han, R., & Li, Z. (2020). Association of growth traits with a structural variation downstream of the KCNJ11 gene: A large population‐based study in chickens. British Poultry Science, 61(3), 320–327.

Wang, Y., Li, J., Feng, C., Zhao, Y., Hu, X., & Li, N. (2017). Transcriptome analysis of comb and testis from rose‐comb silky chicken (R1/R1) and Beijing fatty wild type chicken (r/r). Poultry Science, 96(6), 1866–1873.

Wang, Z., Qu, L., Yao, J., Yang, X., Li, G., Zhang, Y., Li, J., Wang, X., Bai, J., Xu, G., Deng, X., Yang, N., & Wu, C. (2013). An EAV‐HP insertion in 5′ flanking region of SLCO1B3 causes blue eggshell in the chicken. PLoS Genetics, 9(1), e1003183.

Warren, W. C., Hillier, L. W., Tomlinson, C., Minx, P., Kremitzki, M., Graves, T., Markovic, C., Bouk, N., Pruitt, K. D., Thibaud‐Nissen, F., Schneider, V., Mansour, T. A., Brown, C. T., Zimin, A., Hawken, R., Abrahamsen, M., Pyrkosz, A. B., Morisson, M., Fillon, V., … Cheng, H. H. (2017). A new chicken genome assembly provides insight into avian genome structure. G3: Genes, Genomes, Genetics, 7(1), 109–117.

Wei, C., Hou, D., Feng, Y., Li, T., Jing, Z., Li, W., Han, R., Li, G., Sun, G., Tian, Y., Liu, X., Kang, X., & Li, Z. (2020). Molecular characterization and a duplicated 31‐bp indel within the LDB2 gene and its associations with production performance in chickens. Gene, 761, 145046.

Weissensteiner, M. H., Bunikis, I., Catalán, A., Francoijs, K. J., Knief, U., Heim, W., Peona, V., Pophaly, S. D., Sedlazeck, F. J., Suh, A., Warmuth, V. M., & Wolf, J. B. W. (2020). Discovery and population genomics of structural variation in a songbird genus. Nature Communications, 11(1), 3403.

Wellenreuther, M., Mérot, C., Berdan, E., & Bernatchez, L. (2019). Going beyond SNPs: The role of structural genomic variants in adaptive evolution and species diversification. Molecular Ecology, 28(6), 1203–1209.

Wragg, D., Mwacharo, J. M., Alcalde, J. A., Wang, C., Han, J. L., Gongora, J., Gourichon, D., Tixier‐Boichard, M., & Hanotte, O. (2013). Endogenous retrovirus EAV‐HP linked to blue egg phenotype in Mapuche fowl. PLoS One, 8(8), e71393.

Wright, D., Boije, H., Meadows, J. R., Bed'hom, B., Gourichon, D., Vieaud, A., Tixier‐Boichard, M., Rubin, C. J., Imsland, F., Hallböök, F., & Andersson, L. (2009). Copy number variation in intron 1 of SOX5 causes the pea‐comb phenotype in chickens. PLoS Genetics, 5(6), e1000512.

Xu, Y., Hu, J., Fan, W., Liu, H., Zhang, Y., Guo, Z., Huang, W., Liu, X., & Hou, S. (2022). Genome‐wide association analysis reveals 6 copy number variations associated with the number of cervical vertebrae in Pekin ducks. Frontiers in Cell and Developmental Biology, 10, 1041088.

Yang, K. X., Zhou, H., Ding, J. M., He, C., Niu, Q., Gu, C. J., Zhou, Z. X., Meng, H., & Huang, Q. Z. (2020). Copy number variation in HOXB7 and HOXB8 involves in the formation of beard trait in chickens. Animal Genetics, 51(6), 958–963.

Yang, Z., Zou, L., Sun, T., Xu, W., Zeng, L., Jia, Y., Jiang, J., Deng, J., & Yang, X. (2021). Genome‐wide association study using whole‐genome sequencing identifies a genomic region on chromosome 6 associated with comb traits in Nandan‐Yao chicken. Frontiers in Genetics, 12, 682501.

Yuan, X., Cui, H., Jin, Y., Zhao, W., Liu, X., Wang, Y., Ding, J., Liu, L., Wen, J., & Zhao, G. (2022). Fatty acid metabolism‐related genes are associated with flavor‐presenting aldehydes in Chinese local chicken. Frontiers in Genetics, 13, 902180.

Zhang, G., Li, C., Li, Q., Li, B., Larkin, D. M., Lee, C., Storz, J. F., Antunes, A., Greenwold, M. J., Meredith, R. W., Ödeen, A., Cui, J., Zhou, Q., Xu, L., Pan, H., Wang, Z., Jin, L., Zhang, P., Hu, H., … Wang, J. (2014). Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215), 1311–1320.

Zhang, H., Du, Z. Q., Dong, J. Q., Wang, H. X., Shi, H. Y., Wang, N., Wang, S. Z., & Li, H. (2014). Detection of genome‐wide copy number variations in two chicken lines divergently selected for abdominal fat content. BMC Genomics, 15, 1–12.

Zhang, J., Nie, C., Zhang, X., Zhao, X., Jia, Y., Han, J., Chen, Y., Wang, L., Lv, X., Yang, W., Li, K., Zhang, J., Ning, Z., Bao, H., Li, J., Zhao, C., & Qu, L. (2022). A ~4.1 kb deletion in IRX1 gene upstream is completely associated with rumplessness in Piao chicken. Genomics, 114(6), 110515.

Zhang, L., Reifová, R., Halenková, Z., & Gompert, Z. (2021). How important are structural variants for speciation? Genes, 12(7), 1084.

Zhou, Z., Li, M., Cheng, H., Fan, W., Yuan, Z., Gao, Q., Xu, Y., Guo, Z., Zhang, Y., Hu, J., Liu, H., Liu, D., Chen, W., Zheng, Z., Jiang, Y., Wen, Z., Liu, Y., Chen, H., Xie, M., … Jiang, Y. (2018). An intercross population study reveals genes associated with body size and plumage color in ducks. Nature Communications, 9(1), 2648.

Zhu, F., Yin, Z. T., Wang, Z., Smith, J., Zhang, F., Martin, F., Ogeh, D., Hincke, M., Lin, F. B., Burt, D. W., Zhou, Z. K., Hou, S. S., Zhao, Q. S., Li, X. Q., Ding, S. R., Li, G. S., Yang, F. X., Hao, J. P., Zhang, Z., … Hou, Z. C. (2021). Three chromosome‐level duck genome assemblies provide insights into genomic variation during domestication. Nature Communications, 12(1), 5932.

Zhu, T., Liu, M., Peng, S., Zhang, X., Chen, Y., Lv, X., Yang, W., Li, K., Zhang, J., Wang, H., Li, H., Ning, Z., Wang, L., & Qu, L. (2022). A deletion upstream of SOX10 causes light yellow plumage colour in chicken. Genes, 13(2), 327.