Skip to main content
Log in

The serotonin transporter gene could play a role in anti-predator behaviour in a forest passerine

  • Article
  • Published:
Journal of Ethology Aims and scope Submit manuscript

Abstract

Elucidating associations between behavioural variation and genes may help to understand the co-existence of different behavioural phenotypes in natural populations. In birds, two main candidate genes are known to affect exploratory and risk-taking behaviour through the neurotransmitter system: the dopamine receptor D4 gene (DRD4) and the serotonin transporter gene (SERT/SLC6A4). In a small passerine bird, the great tit (Parus major), anti-predator responses (hissing or non-hissing behavioural type) towards a nest predator differ consistently between individuals. As defensive anti-predator behaviours are likely related to variations in neurotransmitter systems, we tested the associations between polymorphisms of the two candidate genes (SERT and DRD4) and the propensity to give hissing calls towards a nest predator in incubating female great tits. We found that acoustic anti-predator responses in wild birds were linked to a single-nucleotide polymorphism in the SERT gene (SNP187 in exon 1), but not in the DRD4 gene. The polymorphism in the SERT gene explains about 16% of the total variance in hissing behaviour. However, as the sample size in this study is quite small, these results are preliminary and should be replicated in future studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abe H, Takeuchi H, Yamada S, Nakamura A, Nagao K, Nirasawa K et al (2013) Characterization of the intronic VNTR polymorphisms found in a paralog of chicken serotonin transporter gene. J Anim Sci 84:281–288

    CAS  Google Scholar 

  • Bize P, Diaz C, Lindström J (2012) Experimental evidence that adult anti-predator behaviour is heritable and not influenced by behavioural copying in a wild bird. Proc R Soc Lond B 279:1380–1388

    Google Scholar 

  • Borgmann KL, Conway CJ, Morrison ML (2013) Breeding phenology of birds: mechanisms underlying seasonal declines in the risk of nest predation. PLoS One 8:e65909

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buitenhuis AJ, Kjaer JB, Labouriau R, Juul-Madsen HR (2006) Altered circulating levels of serotonin and immunological changes in laying hens divergently selected for feather pecking behaviour. Poultry Sci 85:1722–1728

    CAS  Google Scholar 

  • Carere C, Maestripieri D (2013) Animal personalities: behaviour, physiology, and evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Caro T (2005) Anti-predator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301(5631):386–389

    CAS  PubMed  Google Scholar 

  • Chamary JV, Parmley JL, Hurst LD (2006) Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet 7(2):98

    CAS  PubMed  Google Scholar 

  • Cheng HW, Jefferson L (2008) Different behavioural and physiological responses in two genetic lines of laying hens after transportation. Poultry Sci 87:885–892

    Google Scholar 

  • Ebstein RP, Novick O, Umansky R, Priel B, Osher Y, Blaine D et al (1996) Dopamine D4 receptor (D4DR) exon III polymorphisms associated with the human personality trait of Novelty Seeking. Nat Genet 12:78–80

    CAS  PubMed  Google Scholar 

  • Edwards HA, Hajduk GK, Durieux G, Burke T, Dugdale HL (2015) No association between personality and candidate gene polymorphisms in a wild bird population. PloS One 10:10

    Google Scholar 

  • Ernst M, Plate RC, Carlisi CO, Gorodetsky E, Goldman D, Pine DS (2014) Loss aversion and 5HTT gene variants in adolescent anxiety. Develop Cogn Neurosci 8:77–85

    Google Scholar 

  • Fidler AE, van Oers K, Drent PJ, Kuhn S, Müller JC, Kempenaers B (2007) Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc R Soc Lond B 274:1619

    Google Scholar 

  • Fiskerstrand CE, Lovejoy EA, Quinn JP (1999) An intronic polymorphic domain has allele dependent differential enhancer activity in embryonic stem cells. FEBS Lett 458:171–174

    CAS  PubMed  Google Scholar 

  • Flisikowski K, Schwarzenbacher H, Wysocki M, Weigend S, Preisinger R, Kjaer JB et al (2009) Variation in neighbouring genes of the dopaminergic and serotonergic systems affects feather pecking behaviour of laying hens. Anim Genet 40:192–199

    CAS  PubMed  Google Scholar 

  • Garamszegi LZ, Müller JC, Markó G, Szász E, Zsebők S, Herczeg G et al (2014) The relationship between DRD4 polymorphisms and phenotypic correlations of behaviours in the collared flycatcher. Ecol Evol 4(8):1466–1479

    PubMed  PubMed Central  Google Scholar 

  • Gaunt TR, Rodríguez S, Day IN (2007) Cubic exact solutions for the estimation of pairwise haplotype frequencies: implications for linkage disequilibrium analyses and a web tool 'CubeX'. BMC Bioinform 8(1):428

    Google Scholar 

  • Girault JA, Greengard P (2004) The neurobiology of dopamine signaling. Arch Neurol 61:641–644

    PubMed  Google Scholar 

  • Hariri AR, Holmes A (2006) Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn Sci 10(4):182–191

    PubMed  Google Scholar 

  • Hashimoto S, Inoue T, Koyama T (1996) Serotonin reuptake inhibitors reduce conditioned fear stress-induced freezing behaviour in rats. Psychopharmacology 123(2):182–186

    CAS  PubMed  Google Scholar 

  • Holtmann B, Grosser S, Lagisz M, Johnson S, Santos ES, Lara CE et al (2016) Population differentiation and behavioural association of the two ‘personality’ genes DRD4 and SERT in dunnocks (Prunella modularis). Mol Ecol 25:706–722

    CAS  PubMed  Google Scholar 

  • Johnson Z, Brent L, Alvarenga JC, Comuzzie AG, Shelledy W, Ramirez S et al (2015) Genetic influences on response to novel objects and dimensions of personality in papio baboons. Behav Genet 45(2):215–227

    PubMed  PubMed Central  Google Scholar 

  • Kluen E, Kuhn S, Kempenaers B, Brommer JE (2012) A simple cage test captures intrinsic differences in aspects of personality across individuals in a passerine bird. Anim Beh 84(1):279–287

    Google Scholar 

  • Koosa K, Tilgar V (2016) Is hissing behaviour of incubating great tits related to reproductive investment in the wild? Acta Ethol 19:173–180

    Google Scholar 

  • Korsten P, Müller JC, Hermannstädter C, Bouwman KM, Dingemanse NJ, Drent PJ 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

    CAS  PubMed  Google Scholar 

  • Krams I, Vrublevska J, Koosa K, Krama T, Mierauskas P, Rantala MJ et al (2014) Hissing calls improve survival in incubating female great tits (Parus major). Acta Ethol 17:83–88

    Google Scholar 

  • Kreek MJ, Nielsen DA, Butelman ER, LaForge KS (2005) Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction. Nat Neurosci 8:1450–1457

    CAS  PubMed  Google Scholar 

  • Laine V, Gossmann TI, Schachtschneider KM, Garroway CJ, Madsen O, Verhoeven KJ et al (2015) Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat Commun 7:10474

    Google Scholar 

  • Lambrechts MM, Caro S, Charmantier A, Gross N, Galan MJ, Perret P et al (2004) Habitat quality as a predictor of spatial variation in blue tit reproductive performance: a multi-plot analysis in a heterogeneous landscape. Oecologia 141:555–561

    PubMed  Google Scholar 

  • Lesch K-P, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J et al (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274:1527–1531

    CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lima SL (2009) Predators and the breeding bird: behavioural and reproductive flexibility under the risk of predation. Biol Rev 84:485–513

    PubMed  Google Scholar 

  • Lin Z, Walther D, Yu XY, Drgon T, Uhl GR (2004) The human serotonin receptor 2B: coding region polymorphisms and association with vulnerability to illegal drug abuse. Pharmacogene Genom 14:805–811

    CAS  Google Scholar 

  • Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behaviour. Behav Ecol 16(5):945–956

    Google Scholar 

  • Mänd R, Tilgar V, Lõhmus A, Leivits A (2005) Providing nest boxes for hole-nesting birds—does habitat matter? Biodivers Conserv 14:1823–1840

    Google Scholar 

  • Müller JC, Partecke J, Hatchwell BJ, Gaston KJ, Evans KL (2013) Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol Ecol 22:3629–3637

    Google Scholar 

  • Müller JC, Edelaar P, Carrete M, Serrano D, Potti J, Blas J et al (2014) Behaviour-related DRD4 polymorphisms in invasive bird populations. Mol Ecol 23:2876–2885

    Google Scholar 

  • Munafò MR, Clark TG, Moore LR, Payne E, Walton R, Flint J (2003) Genetic polymorphisms and personality in healthy adults: a systematic review and meta-analysis. Mol Psych 8:471–484

    Google Scholar 

  • Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, Makarov SS, Maixner W, Diatchenko L (2006) Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 314:1930–1933

    CAS  PubMed  Google Scholar 

  • Perrins CM (1979) British tits 62. HarperCollins, New York

    Google Scholar 

  • Phi-van L, Holtz M, Kjaer JB, van Phi VD, Zimmermann K (2014) A functional variant in the 5’-flanking region of the chicken serotonin transporter gene is associated with increasing body weight and locomotor activity. J Neurochem 131:12–30

    CAS  PubMed  Google Scholar 

  • Popova NK (1997) Brain serotonin in genetically defined defensive behaviour. Complex Brain Functions 1:309

    Google Scholar 

  • Riyahi S, Sánchez-Delgado M, Calafell F, Monk D, Senar JC (2015) Combined epigenetic and intraspecific variation of the DRD4 and SERT genes influence novelty seeking behaviour in great tit Parus major. Epigenetics 10(6):516–525

    PubMed  PubMed Central  Google Scholar 

  • Rodriguez S, Gaunt TR, Day IN (2009) Hardy-Weinberg equilibrium testing of biological ascertainment for Mendelian randomization studies. Am J Epidem 169(4):505–514

    Google Scholar 

  • Sauna Z, Kimchi-Sarfaty C (2011) Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet 12:683–691

    CAS  PubMed  Google Scholar 

  • Serretti A, Calati R, Mandelli L, De Ronchi D (2006) Serotonin transporter gene variants and behaviour: a comprehensive review. Curr Drug Targets 7:1659–1669

    CAS  PubMed  Google Scholar 

  • Shabalina SA, Spiridonov NA, Kashina A (2013) Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity. Nucleic Acids Res 41:2073–2094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siever LJ (2008) Neurobiology of aggression and violence. Am J Psychiat 165:429–442

    PubMed  Google Scholar 

  • Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B 272(1581):2627–2634

    Google Scholar 

  • Tilgar V, Kikas K (2009) Is parental risk taking negatively related to the level of brood reduction? An experiment with pied flycatchers. Anim Behav 77(1):43–47

    Google Scholar 

  • Timm K, Tilgar V, Saag P (2015) DRD4 gene polymorphism in great tits: gender-specific association with behavioural variation in the wild. Behav Ecol Sociobiol 69:729–735

    Google Scholar 

  • Timm K, van Oers K, Tilgar V (2018) SERT gene polymorphisms are associated with risk-taking behaviour and breeding parameters in wild great tits. J Exp Biol 21:jeb-171595

    Google Scholar 

  • Van Dongen W, Robinson RW, Weston MA, Mulder RA, Guay P-J (2015) Variation at the DRD4 locus is associated with wariness and local site selection in urban black swans. BMC Evol Biol 5:253

    Google Scholar 

  • Van Oers K, Drent PJ, De Goede P, Van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73

    Google Scholar 

  • Van Oers K, De Jong G, Van Noordwijk AJ, Kempenaers N, Drent PJ (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142:9–10

    Google Scholar 

  • Verhulst EC, Mateman AC, Zwier MV, Caro SP, Verhoeven KJ, Oers K (2016) Evidence from pyrosequencing indicates that natural variation in animal personality is associated with DRD4 DNA methylation. Mol Ecol 25:1801–1811

    CAS  PubMed  Google Scholar 

  • Wolf M, Van Doorn S, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Kees van Oers for help with the great tit genome and Jüri Parik for help with molecular analysis. This study was supported by the Estonian Ministry of Education and Research (institutional research funding IUT number 34–8).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vallo Tilgar.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Human and animal rights statement

Birds were ringed under Estonian Department of the Environment Licence No. 11, and blood samples were taken under Animal Procedures Committee of the Estonian Ministry of Agriculture Licence No. 100.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Timm, K., Koosa, K. & Tilgar, V. The serotonin transporter gene could play a role in anti-predator behaviour in a forest passerine. J Ethol 37, 221–227 (2019). https://doi.org/10.1007/s10164-019-00593-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10164-019-00593-7

Keywords

Navigation