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Genetic Architecture of Innate Fear Behavior in Chickens

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Abstract

The genetic architecture of innate fear behavior in chickens is poorly understood. Here, we performed quantitative trait loci (QTL) analysis of innate responses to tonic immobility (TI) and open field (OF) fears in 242 newly hatched chicks of an F2 population between the native Japanese Nagoya breed and the White Leghorn breed using 881 single nucleotide polymorphism markers obtained by restriction site-associated DNA sequencing. At genome-wide 5% significance levels, four QTL for TI traits were revealed on chromosomes 1–3 and 24. Two of these loci had sex-specific effects on the traits. For OF traits, three QTL were revealed on chromosomes 2, 4 and 7. The TI and OF QTL identified showed no overlaps in genomic regions and different modes of inheritance. The three TI QTL and one OF QTL exerted antagonistic effects on the traits. The results demonstrated that context-dependent QTL underlie the variations in innate TI and OF behaviors.

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References

  • Abe H, Nagao K, Nakamura A, Inoue-Murayama M (2013) Differences in responses to repeated fear-relevant stimuli between Nagoya and White Leghorn chicks. Behav Processes 99:95–99

    Article  PubMed  Google Scholar 

  • Ankra-Badu GA, Shriner D, Le Bihan-Duval E, Mignon-Grasteau S, Pitel F, Beaumont C, Duclos MJ, Simon J, Porter TE, Vignal A, Cogburn LA, Allison DB, Yi N, Aggrey SE (2010) Mapping main, epistatic and sex-specific QTL for body composition in a chicken population divergently selected for low or high growth rate. BMC Genomics 11:107

    Article  PubMed  PubMed Central  Google Scholar 

  • Benowitz KM, Coleman JM, Matzkin LM (2019) Assessing the architecture of Drosophila mojavensis locomotor evolution with bulk segregant analysis. G3 9(5):1767–1775

    Article  PubMed  PubMed Central  Google Scholar 

  • Broman KW, Sen S (2009) A Guide to QTL Mapping with R/qtl. Springer, New York

    Book  Google Scholar 

  • Buitenhuis AJ, Rodenburg TB, Siwek M, Cornelissen SJB, Nieuwland MGB, Crooijmans RPMA, Groenen MAM, Koene P, Bovenhuis H, Van Der Poel JJ (2004) Identification of QTLs involved in open-field behavior in young and adult laying hens. Behav Genet 34(3):325–333

    Article  PubMed  Google Scholar 

  • Campler M, Jöngren M, Jensen P (2009) Fearfulness in red junglefowl and domesticated White Leghorn chickens. Behav Processes 81(1):39–43

    Article  PubMed  Google Scholar 

  • Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140

    Article  PubMed  PubMed Central  Google Scholar 

  • Ericsson M, Jensen P (2016) Domestication and ontogeny effects on the stress response in young chickens (Gallus gallus). Sci Rep 6:35818

    Article  PubMed  PubMed Central  Google Scholar 

  • Eriksson J, Larson G, Gunnarsson U, Bed'hom B, Tixier-Boichard M, Strömstedt L, Wright D, Jungerius A, Vereijken A, Randi E, Jensen P, Andersson L (2008) Identification of the Yellow Skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet 4(2):e1000010

    Article  PubMed  PubMed Central  Google Scholar 

  • Fallahsharoudi A, de Kock N, Johnsson M, Bektic L, Ubhayasekera SJKA, Bergquist J, Wright D, Jensen P (2017) Genetic and targeted eQTL mapping reveals strong candidate genes modulating the stress response during chicken domestication. G3 7(2):497–504

    Article  PubMed  Google Scholar 

  • Flint J (2003) Analysis of quantitative trait loci that influence animal behaviour. J Neurobiol 54(1):46–77

    Article  PubMed  Google Scholar 

  • Fogelholm J, Inkabi S, Höglund A, Abbey-Lee R, Johnsson M, Jensen P, Henriksen R, Wright D (2019) Genetical genomics of tonic immobility in the chicken. Genes 10(5):341

    Article  PubMed Central  Google Scholar 

  • Grams V, Bögelein S, Grashorn MA, Bessei W, Bennewitz J (2015) Quantitative genetic analysis of traits related to fear and feather pecking in laying hens. Behav Genet 45(2):228–235

    Article  PubMed  Google Scholar 

  • Hedlund L, Whittle R, Jensen P (2019) Effects of commercial hatchery processing on short- and long-term stress responses in laying hens. Sci Rep 9:2367

    Article  PubMed  PubMed Central  Google Scholar 

  • Hodge CW, Raber J, McMahon T, Walter H, Sanchez-Perez AM, Olive MF, Mehmert K, Morrow AL, Messing RO (2002) Decreased anxiety-like behavior, reduced stress hormones, and neurosteroid supersensitivity in mice lacking protein kinase Cε. J Clin Invest 110(7):1003–1010

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu ZL, Park CA, Reecy JM (2019) Building a livestock genetic and genomic information knowledgebase through integrative developments of animal QTLdb and CorrDB. Nucleic Acids Res 47(D1):D701–D710

    Article  PubMed  Google Scholar 

  • Iffland H, Wellmann R, Preuß S, Tetens J, Bessei W, Piepho HP, Bennewitz J (2020) A novel model to explain extreme feather pecking behavior in laying hens. Behav Genet 50(1):41–50

    Article  PubMed  Google Scholar 

  • Ishikawa A, Kim E-H, Bolor H, Mollah MBR, Namikawa T (2007) A growth QTL (Pbwg1) region of mouse chromosome 2 contains closely linked loci affecting growth and body composition. Mamm Genome 18(4):229–239

    Article  PubMed  Google Scholar 

  • Johnsson M, Williams MJ, Jensen P, Wright D (2016) Genetical genomics of behavior: a novel chicken genomic model for anxiety behavior. Genetics 202(1):327–340

    Article  PubMed  Google Scholar 

  • Kenney-Hunt JP, Vaughn TT, Pletscher LS, Peripato A, Routman E, Cothran K, Durand D, Norgard E, Perel C, Cheverud JM (2006) Quantitative trait loci for body size components in mice. Mamm Genome 17(6):526–537

    Article  PubMed  Google Scholar 

  • Lutz V, Stratz P, Preuß S, Tetens J, Grashorn M, Bessei W, Bennewitz J (2017) A genome-wide association study in a large F2-cross of laying hens reveals novel genomic regions associated with feather pecking and aggressive pecking behavior. Genet Sel Evol 49:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Mackay TFC (2001) Quantitative trait loci in Drosophila. Nat Rev Genet 2(1):11–20

    Article  PubMed  Google Scholar 

  • Mackay TFC (2014) Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet 15(1):22–33

    Article  PubMed  Google Scholar 

  • Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12(12):930–932

    Article  PubMed  Google Scholar 

  • Matteri R, Carroll J, Dyer C (2000) Neuroendocrine responses to stress. In: Moberg GP, Mench JA (eds) The biology of animal stress. CABI Publishing, Wallingford, pp 43–76

    Google Scholar 

  • Mollah MBR, Ishikawa A (2011) Intersubspecific subcongenic mouse strain analysis reveals closely linked QTLs with opposite effects on body weight. Mamm Genome 22(5–6):282–289

    Article  PubMed  Google Scholar 

  • Peters J, Lebrasseur O, Deng H, Larson G (2016) Holocene cultural history of Red jungle fowl (Gallus gallus) and its domestic descendant in East Asia. Quaternary Sci Rev 142:102–119

    Article  Google Scholar 

  • Sakaguchi M, Ishikawa A (2020) Tonic immobility and open field responses in Nagoya, White Leghorn and White Plymouth Rock chicks. J Poult Sci 57(3):183–191

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakaguchi S, Sugino T, Tsumura Y, Ito M, Crisp MD, Bowman DMJS, Nagano AJ, Honjo MN, Yasugi M, Kudoh H, Matsuki Y, Suyama Y, Isagi Y (2015) High-throughput linkage mapping of Australian white cypress pine (Callitris glaucophylla) and map transferability to related species. Tree Genet Genomes 11(6):121

    Article  Google Scholar 

  • Schütz KE, Kerje S, Jacobsson L, Forkman B, Carlborg Ö, Andersson L, Jensen P (2004) Major growth QTLs in fowl are related to fearful behavior: possible genetic links between fear responses and production traits in a red junglefowl × White Leghorn intercross. Behav Genet 34(1):121–130

    Article  PubMed  Google Scholar 

  • Silva A, Paylor R, Wehner J, Tonegawa S (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257(5067):206–211

    Article  PubMed  Google Scholar 

  • Suzuki S, Kobayashi M, Murai A, Tsudzuki M, Ishikawa A (2019) Characterization of growth, fat deposition, and lipid metabolism-related gene expression in lean and obese meat-type chickens. J Poult Sci 56(2):101–111

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsudzuki M (2003) Japanese native chickens. In: Chang H-L, Huang Y-C (eds) The relationships between indigenous animals and humans in the APEC region. The Chinese Society of Animal Science, Chinese Taipei, pp 91–116

    Google Scholar 

  • Wirén A, Jensen P (2011) A growth QTL on chicken chromosome 1 affects emotionality and sociality. Behav Genet 41(2):303–311

    Article  PubMed  Google Scholar 

  • Xu S (2003) Theoretical basis of the Beavis effect. Genetics 165(4):2259–2268

    PubMed  PubMed Central  Google Scholar 

  • Zuidhof MJ, Schneider BL, Carney VL, Korver DR, Robinson FE (2014) Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005. Poult Sci 93(12):2970–2982

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank a member of our laboratory in Nagoya University for help in animal care.

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Authors and Affiliations

  1. Laboratory of Animal Genetics and Breeding, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan

    Akira Ishikawa, Marina Sakaguchi & Sae Suzuki

  2. Faculty of Agriculture, Ryukoku University, Otsu, Shiga, 520-2194, Japan

    Atsushi J. Nagano

Authors
  1. Akira Ishikawa
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  2. Marina Sakaguchi
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  3. Atsushi J. Nagano
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  4. Sae Suzuki
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Contributions

AI conceived, designed and supervised the experiments. MS, SS and AI prepared the materials. MS collected the data. AJN performed the RAD-seq analysis. MS and AI performed the other analyses. AI wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Akira Ishikawa.

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Conflict of interest

Akira Ishikawa, Marina Sakaguchi, Atsushi J. Nagano and Sae Suzuki declare that they have no conflict of interest.

Human and animal rights and informed consent

All institutional and national guidelines for the care and use of laboratory animals were followed. This study did not include any studies with human participants performed by any of the authors. All chicks used in this study were handled in accordance with the guidelines of the Animal Research Committee of Nagoya University.

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Ishikawa, A., Sakaguchi, M., Nagano, A.J. et al. Genetic Architecture of Innate Fear Behavior in Chickens. Behav Genet 50, 411–422 (2020). https://doi.org/10.1007/s10519-020-10012-0

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  • DOI: https://doi.org/10.1007/s10519-020-10012-0

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