Genetic correlates of individual differences in sleep behavior of free-living great tits (Parus major)

G3: Genes, Genomes, Genetics

Volumn 6, Issue 3, 2016, Pages 599-607

  Stuber, Erica F ^a,c   Baumgartner, Christine ^a   Dingemanse, Niels J ^a,b   Kempenaers, Bart ^a   Mueller, Jakob C ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Candidate gene; Circadian rhythm; Genotype phenotype association; Repeatability; Sleep

Indexed keywords

MELANOCORTIN; MICROSATELLITE DNA;

AANAT GENE; ADCYAP1 GENE; ALLELE; ANIMAL EXPERIMENT; ARTICLE; CACNA1C GENE; CLOCK GENE; CONTROLLED STUDY; CREB1 GENE; GENE; GENE FREQUENCY; GENETIC CORRELATION; GENETIC POLYMORPHISM; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; GRIA3 GENE; HETEROZYGOSITY; MICROSATELLITE MARKER; NIGHT; NONHUMAN; NPAS2 CLOCK GENE; NPSR1 GENE; PARUS MAJOR; PCSK2 GENE; PHENOTYPIC VARIATION; POPULATION STRUCTURE; SLEEP; SLEEP TIME; WAKEFULNESS; ANIMAL; ANIMAL BEHAVIOR; CIRCADIAN RHYTHM; GENETIC ASSOCIATION STUDY; GENETICS; PASSERIFORMES; PHENOTYPE; POPULATION GENETICS;

ALLELES; ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; GENE FREQUENCY; GENETIC ASSOCIATION STUDIES; GENETICS, POPULATION; GENOTYPE; MICROSATELLITE REPEATS; PASSERIFORMES; PHENOTYPE; POLYMORPHISM, GENETIC; SLEEP;

EID: 84959490866     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.024216     Document Type: Article

References (94)

1. Abe, H., and N. J. Gemmell, 2014 Abundance, arrangement, and function of sequence motifs in the chicken promoters. BMC Genomics 15: 900.
2. Acevedo, N., A. Saaf, C. Soderhall, E. Melen, J. Mandelin et al., 2013 Interaction between retinoid acid receptor-related orphan receptor alpha (RORA) and neuropeptide S receptor 1 (NPSR1) in asthma. PLoS One 8(4): e60111.
3. Ambrosius, U., S. Lietzenmaier, R. Wehrle, A. Wichniak, S. Kalus et al., 2008 Heritability of sleep electroencephalogram. Biol. Psychiatry 64(4):344-348.
4. Amlaner, C. J., and N. J. Ball, 1983 A synthesis of sleep in wild birds. Behaviour 87: 85-119.
5. Araya-Ajoy, Y. G., 2015 Multi-level variation in labile characters: adaptive causes and evolutionary consequences. Ph. D. Thesis, Ludwig-Maximilians-Universität, Munich.
6. Bakker, T. C., 1999 The study of intersexual selection using quantitative genetics. Behaviour 136(9): 1237-1266.
7. Balding, D. J., 2006 A tutorial on statistical methods for population association studies. Nat. Rev. Genet. 7(10): 781-791.
8. Bensch, S., T. Price, and J. Kohn, 1997 Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol. Ecol. 6(1): 91-92.
9. Boake, C. R., 1989 Repeatability: its role in evolutionary studies of mating behavior. Evol. Ecol. 3(2): 173-182.
10. Boehmler,W., T. Carr, C. Thisse, B. Thisse, V. A. Canfield et al., 2007 D4 Dopamine receptor genes of zebrafish and effects of the antipsychotic clozapine on larval swimming behaviour. Genes Brain Behav. 6(2): 155-166.
11. Caprioli, M., R. Ambrosini, G. Boncoraglio, E. Gatti, A. Romano et al., 2012 Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow. PLoS One 7(4): e35140.
12. Cassone, V. M., and D. F. Westneat, 2012 The bird of time: cognition and the avian biological clock. Front. Mol. Neurosci. 5: 32.
13. Comings, D. E., R. Gade-Andavolu, N. Gonzalez, S. Wu, D. Muhleman et al., 2000 A multivariate analysis of 59 candidate genes in personality traits: the temperament and character inventory. Clin. Genet. 58(5): 375-385.
14. Costa, L. M., 2009 The behavioral ecology of sleep: examining the influence of exogenous and endogenous factors on sleep modification in the house sparrow, Passer domesticus, Ph. D. Thesis, Princeton University, Princeton, NJ.
15. Dall, S. R. X., A. I. Houston, and J. M. McNamara, 2004 The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol. Lett. 7(8): 734-739.
16. Dawson, D. A., O. Hanotte, C. Greig, I. R. K. Stewart, and T. Burke, 2000 Polymorphic microsatellites in the blue tit Parus caeruleus and their cross-species utility in 20 songbird families. Mol. Ecol. 9(11): 1941-1944.
17. Dochtermann, N. A., and N. J. Dingemanse, 2013 Behavioral syndromes as evolutionary constraints. Behav. Ecol. 24(4): 806-811.
18. Dor, R., I. J. Lovette, R. J. Safran, S. M. Billerman, G. H. Huber et al., 2011 Low variation in the polymorphic clock gene poly-q region despite population genetic structure across barn swallow (Hirundo rustica) populations. PLoS One 6(12): e28843.
19. Double, M. C., D. Dawson, T. Burke, and A. Cockburn, 1997 Finding the fathers in the least faithful bird: a microsatellite-based genotyping system for the superb fairy-wren Malurus cyaneus. Mol. Ecol. 6(7):691-693.
20. Duangdao, D. M., S. D. Clark, N. Okamura, and R. K. Reinscheid, 2009 Behavioral phenotyping of Neuropeptide S receptor knockout mice. Behav. Brain Res. 205(1): 1-9.
21. Earl, D. A., and B. M. Vonholdt, 2012 STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4(2): 359-361.
22. Excoffier, L., and H. E. L. Lischer, 2010 Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10(3): 564-567.
23. Falush, D., M. Stephens, and J. K. Pritchard, 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4): 1567-1587.
24. Ferrara, M., and L. De Gennaro, 2000 The sleep inertia phenomenon during the sleep-wake transition: theoretical and operational issues. Aviat. Space Environ. Med. 71(8): 843-848.
25. Fidler, A. E., K. van Oers, P. J. Drent, S. Kuhn, J. C. Mueller et al., 2007 Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc. Biol. Sci. 274(1619): 1685-1691.
26. Fitzpatrick, M. J., Y. Ben-Shahar, H. M. Smid, L. E. M. Vet, G. E. Robinson et al., 2005 Candidate genes for behavioural ecology. Trends Ecol. Evol. 20(2): 96-104.
27. Franken, P., D. Chollet, and M. Tafti, 2001 The homeostatic regulation of sleep need is under genetic control. J. Neurosci. 21(8): 2610-2621.
28. Gadberry, M. D., S. T. Malcomber, A. N. Doust, and E. A. Kellogg, 2005 Primaclade-a flexible tool to find conserved PCR primers across multiple species. Bioinformatics 21(7): 1263-1264.
29. Gelman, A., and J. Hill, 2007 Data analysis using regression and multilevel-/hierarchical models, Cambridge University Press, Cambridge, UK.
30. Gelman, A., J. Hill, Y.-S. Su, et al., 2015 arm: Data analysis using regression and multi-level/hierarchical models. Available at: http://CRAN.R-project.org/package=arm.
31. Gottlieb, D. J., G. T. O'Connor, and J. B. Wilk, 2007 Genome-wide association of sleep and circadian phenotypes. BMC Med. Genet. 8: Suppl 1:S9.
32. Hallgrímsson, B., and B. K. Hall, 2011 Variation: a central concept in biology, Academic Press, New York.
33. Hammock, E. A. D., and L. J. Young, 2004 Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol. Biol. Evol. 21(6): 1057-1063.
34. Imagawa, M., Y. Ishikawa, H. Shimano, S. Osada, and T. Nishihara, 1995 CTG triplet repeat in mouse growth-inhibitory factor metallothionein-III gene promoter represses the transcriptional activity of the heterologous promoters. J. Biol. Chem. 270(36): 20898-20900.
35. Johnsen, A., A. E. Fidler, S. Kuhn, K. L. Carter, A. Hoffmann et al., 2007 Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol. Ecol. 16(22): 4867-4880.
36. Jones, S. G., V. V. Vyazovskiy, C. Cirelli, G. Tononi, and R. M. Benca, 2008 Homeostatic regulation of sleep in the white-crowned sparrow (Zonotrichia leucophrys gambelii). BMC Neurosci. 9(1): 47.
37. Jorgensen, T. J., I. Ruczinski, B. Kessing, M. W. Smith, Y. Y. Shugart et al., 2009 Hypothesis-driven candidate gene association studies: practical design and analytical considerations. Am. J. Epidemiol. 170(8): 986-993.
38. Juhasz, G., D. Chase, E. Pegg, D. Downey, Z. G. Toth et al., 2009 CNR1 gene is associated with high neuroticism and low agreeableness and interacts with recent negative life events to predict current depressive symptoms. Neuropsychopharmacology 34(8): 2019-2027.
39. Kang, S. W., A. Thayananuphat, T. Bakken, and M. E. El Halawani, 2007 Dopamine-melatonin neurons in the avian hypothalamus controlling seasonal reproduction. Neuroscience 150(1): 223-233.
40. Korsten, P., J. C.Mueller,C.Hermannstadter, K.M. Bouwman,N. J. Dingemanse et al., 2010 Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations. Mol. Ecol. 19(4):832-843.
41. Koslowsky, M., and H. Babkoff, 1992 Metaanalysis of the relationship between total sleep-deprivation and performance. Chronobiol. Int. 9(2):132-136.
42. Lakin-Thomas, P. L., 2000 Circadian rhythms-new functions for old clock genes? Trends Genet. 16(3): 135-142.
43. Laposky, A. D., J. Bass, A. Kohsaka, and F. W. Turek, 2008 Sleep and circadian rhythms: key components in the regulation of energy metabolism. FEBS Lett. 582(1): 142-151.
44. Lesku, J. A., A. L. Vyssotski, D. Martinez-Gonzalez, C. Wilzeck, and N. C. Rattenborg, 2011 Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds? Proc. R. Soc. Lond. B Biol. Sci. 278: 2419-2428.
45. Lesku, J. A., N. C. Rattenborg, M. Valcu, A. L. Vyssotski, S. Kuhn et al., 2012 Adaptive sleep loss in polygynous pectoral sandpipers. Science 337(6102): 1654-1658.
46. Liedvogel, M., and B. C. Sheldon, 2010 Low variability and absence of phenotypic correlates of Clock gene variation in a great tit Parus major population. J. Avian Biol. 41(5): 543-550.
47. Liedvogel, M., C. K. Cornwallis, and B. C. Sheldon, 2012 Integrating candidate gene and quantitative genetic approaches to understand variation in timing of breeding in wild tit populations. J. Evol. Biol. 25(5): 813-823.
48. Lowe, W. L., and T. E. Reddy, 2015 Genomic approaches for understanding the genetics of complex disease. Genome Res. 25(10): 1432-1441.
49. Meis, S., J. R. Bergado-Acosta, Y. Yanagawa, K. Obata, O. Stork et al., 2008 Identification of a neuropeptide S responsive circuitry shaping amygdala activity via the endopiriform nucleus. PLoS One 3(7): e2695.
50. Moran, N. A., 1992 The evolutionary maintenance of alternative phenotypes. Am. Nat. 139(5): 971-989.
51. Mousseau, T. A., B. Sinervo, and J. A. Endler, 2000 Adaptive genetic variation in the wild, Oxford University Press, New York.
52. Mueller, J. C., F. Pulido, and B. Kempenaers, 2011 Identification of a gene associated with avian migratory behaviour. Proceedings of the Royal Society B-Biological Sciences 278: 2848-2856.
53. Mueller, J. C., J. Partecke, B. J. Hatchwell, K. J. Gaston, and K. L. Evans, 2013 Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol. Ecol. 22(13): 3629-3637.
54. Mueller, J. C., P. Edelaar, M. Carrete, D. Serrano, J. Potti et al., 2014 Behaviour-related DRD4 polymorphisms in invasive bird populations. Mol. Ecol. 23(11): 2876-2885.
55. Mundy, N. I., 2005 A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc. Biol. Sci. 272(1573): 1633-1640.
56. Nagy, A. D., and V. J. Csernus, 2007 The role of PACAP in the control of circadian expression of clock genes in the chicken pineal gland. Peptides 28(9): 1767-1774.
57. Nakagawa, S., and H. Schielzeth, 2010 Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 85(4): 935-956.
58. Naylor, E., B. M. Bergmann, K. Krauski, P. C. Zee, J. S. Takahashi et al., 2000 The circadian clock mutation alters sleep homeostasis in the mouse. J. Neurosci. 20(21): 8138-8143.
59. Pace-Schott, E. F., and J. A. Hobson, 2002 The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat. Rev. Neurosci. 3(8): 591-605.
60. Parsons, M. J., K. J. Lester, N. L. Barclay, P. M. Nolan, T. C. Eley et al., 2013 Replication of genome-wide association studies (GWAS) loci for sleep in the British G1219 cohort. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 162B(5): 431-438.
61. Partinen, M., J. Kaprio, M. Koskenvuo, P. Putkonen, and H. Langinvainio, 1983 Genetic and environmental determination of human sleep. Sleep 6(3): 179-185.
62. Pieretti, M., F. P. Zhang, Y. H. Fu, S. T. Warren, B. A. Oostra et al., 1991 Absence of expression of the FMR-1 gene in fragile-X syndrome. Cell 66(4): 817-822.
63. Press, M. O., K. D. Carlson, and C. Queitsch, 2014 The overdue promise of short tandem repeat variation for heritability. Trends Genet. 30(11): 504-512.
64. Primmer, C. R., T. Raudsepp, B. P. Chowdhary, A. P. Moller, and H. Ellegren, 1997 Low frequency of microsatellites in the avian genome. Genome Res. 7(5): 471-482.
65. Pritchard, J. K., M. Stephens, and P. Donnelly, 2000 Inference of population structure using multilocus genotype data. Genetics 155(2): 945-959.
66. R Development Core Team, 2011 R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.
67. Réale, D., S. M. Reader, D. Sol, P. T. McDougall, and N. J. Dingemanse, 2007 Integrating animal temperament within ecology and evolution. Biol. Rev. Camb. Philos. Soc. 82(2): 291-318.
68. Saino, N., G. Bazzi, E. Gatti, M. Caprioli, J. G. Cecere et al., 2015 Polymorphism at the Clock gene predicts phenology of long-distance migration in birds. Mol. Ecol. 24(8): 1758-1773.
69. Saladin, V., D. Bonfils, T. Binz, and H. Richner, 2003 Isolation and characterization of 16 microsatellite loci in the Great Tit Parus major. Mol. Ecol. Notes 3(4): 520-522.
70. Sawaya, S., A. Bagshaw, E. Buschiazzo, P. Kumar, S. Chowdhury et al., 2013 Microsatellite tandem repeats are abundant in human promoters and are associated with regulatory elements. PLoS One 8(2): e54710.
71. Scriba, M. F., A. L. Ducrest, I. Henry, A. L. Vyssotski, N. C. Rattenborg et al., 2013 Linking melanism to brain development: expression of a melanism-related gene in barn owl feather follicles covaries with sleep ontogeny. Front. Zool. 10: 42.
72. Shimada, M. K., M. Inoue-Murayama, Y. Ueda, M. Maejima, Y. Murayama et al., 2004 Polymorphism in the second intron of dopamine receptor D4 gene in humans and apes. Biochem. Biophys. Res. Commun. 316(4):1186-1190.
73. Spada, J., C. Sander, R. Burkhardt, M. Hantzsch, R. Mergl et al., 2014 Genetic association of objective sleep phenotypes with a functional polymorphism in the neuropeptide S receptor gene. PLoS One 9(6): e98789.
74. Steinmeyer, C., H. Schielzeth, J. C. Mueller, and B. Kempenaers, 2010 Variation in sleep behaviour in free-living blue tits, Cyanistes caeruleus: effects of sex, age and environment. Anim. Behav. 80(5): 853-864.
75. Steinmeyer, C., B. Kempenaers, and J. C. Mueller, 2012 Testing for associations between candidate genes for circadian rhythms and individual variation in sleep behaviour in blue tits. Genetica 140(4-6): 219-228.
76. Stirling, D. G., D. Reale, and D. A. Roff, 2002 Selection, structure and the heritability of behaviour. J. Evol. Biol. 15(2): 277-289.
77. Stuber, E. F., N. J. Dingemanse, B. Kempenaers, and J. C. Mueller, 2015 Sources of intraspecific variation in sleep behaviour of wild great tits (Parus major). Anim. Behav. 106: 201-221.
78. Szymczak, J., H.-W. Helb, and W. Kaiser, 1993 Electrophysiological and behavioral correlates of sleep in the blackbird (Turdus merula). Physiol. Behav. 53(6): 1201-1210.
79. Tabor, H. K., N. J. Risch, and R. M. Myers, 2002 Candidate-gene approaches for studying complex genetic traits: practical considerations. Nat. Rev. Genet. 3(5): 391-397.
80. Tielbeek, J. J., S. E. Medland, B. Benyamin, E. M. Byrne, A. C. Heath et al., 2012 Unraveling the genetic etiology of adult antisocial behavior: a genome-wide association study. PLoS One 7(10): e45086.
81. Toh, K. L., C. R. Jones, Y. He, E. J. Eide, W. A. Hinz et al., 2001 An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291(5506): 1040-1043.
82. Toth, A. L., and G. E. Robinson, 2007 Evo-devo and the evolution of social behavior. Trends Genet. 23(7): 334-341.
83. Utge, S., P. Soronen, T. Partonen, A. Loukola, E. Kronholm et al., 2010 A population-based association study of candidate genes for depression and sleep disturbance. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 153B(2):468-476.
84. Utge, S., E. Kronholm, T. Partonen, P. Soronen, H. M. Ollila et al., 2011 Shared genetic background for regulation of mood and sleep: association of GRIA3 with sleep duration in healthy Finnish women. Sleep 34(10): 1309-1316.
85. van Oers, K., G. de Jong, A. J. van Noordwijk, B. Kempenaers, and P. J. Drent, 2005 Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142: 1185-1206.
86. van Oers, K., and J. C. Mueller, 2010 Evolutionary genomics of animal personality. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365(1560): 3991-4000.
87. Vaudry, D., A. Falluel-Morel, S. Bourgault, M. Basille, D. Burel et al., 2009 Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol. Rev. 61(3): 283-357.
88. Wang, Y. H., S. Amirhaeri, S. Kang, R. D. Wells, and J. D. Griffith, 1994 Preferential nucleosome assembly at DNA triplet repeats from the myotonic-dystrophy gene. Science 265(5172): 669-671.
89. Wisor, J. P., B. F. O'Hara, A. Terao, C. P. Selby, T. S. Kilduff et al., 2002 A role for cryptochromes in sleep regulation. BMC Neurosci. 3(1): 20.
90. Xu, Y. L., R. K. Reinscheid, S. Huitron-Resendiz, S. D. Clark, Z. W. Wang et al., 2004 Neuropeptide S: a neuropeptide promoting arousal and anxiolytic-like effects. Neuron 43(4): 487-497.
91. Xu, Y., Q. S. Padiath, R. E. Shapiro, C. R. Jones, S. C. Wu et al., 2005 Functional consequences of a CKId mutation causing familial advanced sleep phase syndrome. Nature 434(7033): 640-644.
92. Yoshihara, C., Y. Tashiro, S. Taniuchi, H. Katayama, S. Takahashi et al., 2011 Feather follicles express two classes of pro-opiomelanocortin (POMC) mRNA using alternative promoters in chickens. Gen. Comp. Endocrinol. 171(1): 46-51.
93. Zepelin, H., and A. Rechtschaffen, 1974 Mammalian sleep, longevity, and energy metabolism. Brain Behav. Evol. 10(6): 425-470.
94. Zhou, Z. F., G. S. Zhu, A. R. Hariri, M. A. Enoch, D. Scott et al., 2008 Genetic variation in human NPY expression affects stress response and emotion. Nature 452(7190): 997-1001.