Combined epigenetic and intraspecific variation of the DRD4 and SERT genes influence novelty seeking behavior in great tit Parus major

Epigenetics

Volumn 10, Issue 6, 2015, Pages 516-525

  Riyahi, Sepand ^a   Sánchez Delgado, Marta ^b   Calafell, Francesc ^c   Monk, David ^b   Senar, Juan Carlos ^a  

^a Museu de Zoologia   (Spain)

^b HOSPITAL DURAN I REYNALS   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

DRD4; Methylation; Novelty seeking; Personality traits; SERT; Urbanization

Indexed keywords

DOPAMINE 4 RECEPTOR; GENOMIC DNA; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; CPG ISLAND; DNA METHYLATION; DOPAMINE RECEPTOR D4 GENE; EPIGENETICS; EXON; GENE; INFORMATION SEEKING; INTRASPECIFIC VARIATION; NONHUMAN; PARUS MAJOR; PHENOTYPE; POLYMERASE CHAIN REACTION; PYROSEQUENCING; SCORING SYSTEM; SEROTONIN TRANSPORTER GENE; ALLELE; ANIMAL; EXPLORATORY BEHAVIOR; GENETIC EPIGENESIS; GENETICS; GENOTYPE; PASSERIFORMES; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; ANIMALS; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; EXONS; EXPLORATORY BEHAVIOR; GENOTYPE; PASSERIFORMES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; RECEPTORS, DOPAMINE D4; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84943789417     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2015.1046027     Document Type: Article

References (49)

1. Felthous A, Sass H. International Handbook on Psychopathic Disorders and the Law; Chichester: John Wiley & Sons: 2007; Vol. 1, Diagnosis and Treatment.
2. Reif A, Lesch KP. Toward a molecular architecture of personality. Behav Brain Res 2003; 139(1): 1-20; PMID: 12642172; http://dx. doi. org/10. 1016/S0166-4328(02)00267-X.
3. Bailey JN, Breidenthal SE, Jorgensen MJ, McCracken JT, Fairbanks LA. The association of DRD4 and novelty seeking is found in a nonhuman primate model. Psychiat Genet 2007; 17(1): 23-7; PMID: 17167341; http://dx. doi. org/10. 1097/YPG. 0b013e32801140f2.
4. Van Gestel S, Van Broeckhoven C. Genetics of personality: are we making progress? Mol Psychiat 2003; 8 (10): 840-52; PMID: 14515135; http://dx. doi. org/10. 1038/sj. mp. 4001367.
5. Schinka JA, Letsch EA, Crawford FC. DRD4 and novelty seeking: results of meta-analyses. Am J Med Genet 2002; 114(6): 643-8; PMID: 12210280; http://dx. doi. org/10. 1002/ajmg. 10649.
6. Savitz JB, Ramesar RS. Genetic variants implicated in personality: a review of the more promising candidates. Am J Med Genet Part B: Neuropsychiatr Genet 2004; 131(1): 20-32; PMID: 15389772; http://dx. doi. org/10. 1002/ajmg. b. 20155.
7. Ebstein RP. The molecular genetic architecture of human personality: beyond self-report questionnaires. Mol Psychiat 2006; 11(5): 427-45; PMID: 16534505; http://dx. doi. org/10. 1038/sj. mp. 4001814.
8. Momozawa Y, Takeuchi Y, Kusunose R, Kikusui T, Mori Y. Association between equine temperament and polymorphisms in dopamine D4 receptor gene. Mamm Genome 2005; 16(7): 538-44; PMID: 16151699; http://dx. doi. org/10. 1007/s00335-005-0021-3.
9. Kluger AN, Siegfried Z, Ebstein RP. A meta-analysis of the association between DRD4 polymorphism and novelty seeking. Mol Psychiat 2002; 7(7): 712-7; PMID: 12192615; http://dx. doi. org/10. 1038/sj. mp. 4001082.
10. Fidler AE, van Oers K, Drent PJ, Kuhn S, Mueller JC, Kempenaers B. Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc R Soc Lond B 2007; 274(1619): 1685-91; PMID: 17472912; http://dx. doi. org/10. 1098/rspb. 2007. 0337.
11. Korsten P, Mueller JC, Hermannstadter C, Bouwman KM, Dingemanse NJ, Drent PJ, Liedvogel M, Matthysen E, Van Oers K, Van Overveld T, et al. Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations. Mol Ecol 2010; 19(4): 832-43; PMID: 20070517; http://dx. doi. org/10. 1111/j. 1365-294X. 2009. 04518. x.
12. Mueller JC, Korsten P, Hermannstaedter C, Feulner T, Dingemanse NJ, Matthysen E, van Oers K, van Overveld T, Patrick SC, Quinn JL, et al. Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations. Mol Ecol 2013; 22 (10): 2797-809; PMID: 23506506; http://dx. doi. org/10. 1111/mec. 12282.
13. Mueller JC, Partecke J, Hatchwell BJ, Gaston KJ, Evans KL. Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol Ecol 2013; 22(13): 3629-37; PMID: 23495914; http://dx. doi. org/10. 1111/mec. 12288.
14. Blewitt ME, Vickaryous NK, Paldi A, Koseki H, Whitelaw E. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet 2006; 2(4), e49; PMID: 16604157; http://dx. doi. org/10. 1371/journal. pgen. 0020049.
15. Fusco G, Minelli A. Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans Royal Soc B: Biol Sci 2010; 365(1540): 547-56; PMID: 20083631; http://dx. doi. org/10. 1098/rstb. 2009. 0267.
16. Kucharski R, Maleszka J, Foret S, Maleszka R. Nutritional control of reproductive status in honeybees via DNA methylation. Science 2008; 319(5871): 1827-30; PMID: 18339900; http://dx. doi. org/10. 1126/science. 1153069.
17. Kerkel K, Spadola A, Yuan E, Kosek J, Jiang L, Hod E, Li K, Murty VV, Schupf N, Vilain E. Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation. Nat Genet 2008; 40(7): 904-8; PMID: 18568024; http://dx. doi. org/10. 1038/ng. 174.
18. Leung D, Jung I, Rajagopal N, Schmitt A, Selvaraj S, Lee AY, Yen CA, Lin S, Lin Y, Qiu Y. Integrative analysis of haplotype-resolved epigenomes across human tissues. Nature 2015; 518(7539): 350-4; PMID: 25693566; http://dx. doi. org/10. 1038/nature14217.
19. Schalkwyk LC, Meaburn EL, Smith R, Dempster EL, Jeffries AR, Davies MN, Plomin R, Mill J. Allelic skewing of DNA methylation is widespread across the genome. Am J Hum Genet 2010; 86(2): 196-212; PMID: 20159110; http://dx. doi. org/10. 1016/j. ajhg. 2010. 01. 014.
20. Devlin AM, Brain U, Austin J, Oberlander TF. Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. Plos One 2010; 5(8): e12201; PMID: 20808944; http://dx. doi. org/10. 1371/journal. pone. 0012201.
21. Oberlander TF, Weinberg J, PapsdorfM, GrunauR, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008; 3(2): 97-106; PMID: 18536531; http://dx. doi. org/10. 4161/epi. 3. 2. 6034.
22. Beach SR, Brody GH, Todorov AA, Gunter TD, Philibert RA. Methylation at SLC6A4 is linked to family history of child abuse: an examination of the Iowa Adoptee sample. Am J Med Genet Part B: Neuropsychiatr Genet 2010; 153(2): 710-3.
23. van Mil NH, Steegers-Theunissen RgP, Bouwland-Both MI, Verbiest MM, Rijlaarsdam J, Hofman A, Steegers EA, Heijmans BT, Jaddoe VW, Verhulst FC. DNA methylation profiles at birth and child ADHDsymptoms. J Psychiatr Res 2014; 49: 51-9; PMID: 24290898; http://dx. doi. org/10. 1016/j. jpsychires. 2013. 10. 017.
24. Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A, Moffitt TE, Mill J. A longitudinal study of epigenetic variation in twins. Epigenetics 2010; 5 (6): 516-26; PMID: 20505345; http://dx. doi. org/10. 4161/epi. 5. 6. 12226.
25. Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, Van Schooten FJ, Berndt ML, Pogribny IP, Koturbash I, Williams A. Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc Natl Acad Sci 2008; 105 (2): 605-10; PMID: 18195365; http://dx. doi. org/10. 1073/pnas. 0705896105.
26. Björklund M, Ruiz I, Senar JC. Genetic differentiation in the urban habitat: the great tits (Parus major) of the parks of Barcelona city. Biol J Linn Soc 2010; 99(1): 9-19; PMID: 24843434; http://dx. doi. org/10. 1111/j. 1095-8312. 2009. 01335. x.
27. Senar JC, Conroy MJ, Quesada J, Mateos-Gonzalez F. Selection based on the size of the black tie of the great tit may be reversed in urban habitats. Ecol Evol 2014; 4: 2625-32; PMID: 25077014; http://dx. doi. org/10. 1002/ece3. 999.
28. Drent PJ, Van Oers K, Van Noordwijk AJ. Realized heritability of personalities in the great tit (Parus major). Proc R Soc Lond B 2003; 270: 45-51; PMID: 12590770; http://dx. doi. org/10. 1098/rspb. 2002. 2168.
29. Verbeek MEM, Drent PJ, Wiepkema PR. Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 1994; 48: 1113-21; PMID: 15520517; http://dx. doi. org/10. 1006/anbe. 1994. 1344.
30. Dingemanse NJ, Both C, Drent PJ, Van Oers K, Van Noordwijk AJ. Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 2002; 64: 929-38; PMID: 15002773; http://dx. doi. org/10. 1006/anbe. 2002. 2006.
31. Quinn JL, Patrick SC, Bouwhuis S, Wilkin TA, Sheldon BC. Heterogeneous selection on a heritable temperament trait in a variable environment. J Anim Ecol 2009; 78(6): 1203-15; PMID: 19558612; http://dx. doi. org/10. 1111/j. 1365-2656. 2009. 01585. x.
32. Budaev SV. The statistical analysis of behavioural latency measures. ISCP Newslett 1997; 14: 1-4.
33. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001; 68(4): 978-89; PMID: 11254454; http://dx. doi. org/10. 1086/319501.
34. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009; 25(11): 1451-2; PMID: 19346325; http://dx. doi. org/10. 1093/bioinformatics/btp187.
35. Excoffier L, Laval G, Schneider S. Arlequin. (version 3. 0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 2005; 1: 47-50.
36. Barrett JC, Fry B, Maller JDMJ, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005; 21(2): 263-5; PMID: 15297300; http://dx. doi. org/10. 1093/bioinformatics/bth457.
37. Abe H, Ito S, Inoue-Murayama M. Polymorphisms in the extracellular region of dopamine receptor D4 within and among avian orders. J Mol Evol 2011; 72 (3): 253-64; PMID: 21286696; http://dx. doi. org/10. 1007/s00239-011-9432-9.
38. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, Schübeler D. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007; 39 (4): 457-66; PMID: 17334365.
39. Crews D, Gore AC, Hsu TS, DanglebenNL, Spinetta M, Schallert T, Anway MD, Skinner MK. Transgenerational epigenetic imprints on mate preference. Proc Natl Acad Sci 2007; 104(14): 5942-6; PMID: 17389367; http://dx. doi. org/10. 1073/pnas. 0610410104.
40. Ouellet-Morin I, Wong CCY, Danese A, Pariante CM, Papadopoulos AS, Mill J, Arseneault L. Increased serotonin transporter gene (SERT) DNA methylation is associated with bullying victimization and blunted cortisol response to stress in childhood: a longitudinal study of discordant monozygotic twins. Psychol Med 2013; 43(09): 1813-23; PMID: 23217646; http://dx. doi. org/10. 1017/S0033291712002784.
41. Wong CCY, Caspi A, Williams B, Craig IW, Houts R, Ambler A, Moffitt TE, Mill J. A longitudinal study of epigenetic variation in twins. Epigenetics 2010; 5 (6): 516-26; PMID: 20505345; http://dx. doi. org/10. 4161/epi. 5. 6. 12226.
42. Kinnally EL. Epigenetic plasticity following early stress predicts long-term health outcomes in rhesus macaques. Am J Phys Anthropol 2014; 155(2): 192-9; PMID: 25100197; http://dx. doi. org/10. 1002/ajpa. 22565.
43. Tschirren B, Bensch S. Genetics of personalities: no simple answers for complex traits. Mol Ecol 2010; 19 (4): 624-6; PMID: 20456219; http://dx. doi. org/10. 1111/j. 1365-294X. 2009. 04519. x.
44. Torné-Noguera A, Pagani-Núñez E, Senar JC. Great Tit (Parus major) breath rate in response to handling stress: urban and forest birds differ. J Orn 2014; 155: 315-8; http://dx. doi. org/10. 1007/s10336-013-1025-5.
45. Prezeworski M, Coop G, Wall JD. The signature of positive selection on standing genetic variation. Evolution 2005; 59(11): 2312-23; PMID: 16396172; http://dx. doi. org/10. 1111/j. 0014-3820. 2005. tb00941. x.
46. Bossdorf O, Richards CL, Pigliucci M. Epigenetics for ecologists. Ecol Lett 2008; 11(2): 106-15.
47. Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ. Patterns of population epigenomic diversity. Nature 2013; 495(7440): 193-8; PMID: 23467092; http://dx. doi. org/10. 1038/nature11968.
48. Duncan EJ, Gluckman PD, Dearden PK. Epigenetics, plasticity, and evolution: how do we link epigenetic change to phenotype? J Exp Zool Part B: Mol Dev Evol 2014; 322(4): 208-20; PMID: 24719220; http://dx. doi. org/10. 1002/jez. b. 22571.
49. Rando OJ, Verstrepen KJ. Timescales of genetic and epigenetic inheritance. Cell 2007; 128(4): 655-68; PMID: 17320504; http://dx. doi. org/10. 1016/j. cell. 2007. 01. 023.