Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans

Edited by Solomon H. Snyder, Johns Hopkins University School of Medicine, Baltimore, MD, and approved July 14, 2008
September 16, 2008
105 (37) 14153-14156

Abstract

Pair-bonding has been suggested to be a critical factor in the evolutionary development of the social brain. The brain neuropeptide arginine vasopressin (AVP) exerts an important influence on pair-bonding behavior in voles. There is a strong association between a polymorphic repeat sequence in the 5′ flanking region of the gene (avpr1a) encoding one of the AVP receptor subtypes (V1aR), and proneness for monogamous behavior in males of this species. It is not yet known whether similar mechanisms are important also for human pair-bonding. Here, we report an association between one of the human AVPR1A repeat polymorphisms (RS3) and traits reflecting pair-bonding behavior in men, including partner bonding, perceived marital problems, and marital status, and show that the RS3 genotype of the males also affects marital quality as perceived by their spouses. These results suggest an association between a single gene and pair-bonding behavior in humans, and indicate that the well characterized influence of AVP on pair-bonding in voles may be of relevance also for humans.

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Acknowledgments.

This project was supported by National Institute of Mental Health Grant R01MH54610, Bank of Sweden Tercentenary Foundation Grant J2004–0036:1, and a postdoctoral fellowship sponsored by the Brain Foundation, Sweden (to L.W.).

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References

1
RI Dunbar, S Shultz, Evolution in the social brain. Science 317, 1344–1347 (2007).
2
LJ Young, Z Wang, The neurobiology of pair bonding. Nat Neurosci 7, 1048–1054 (2004).
3
MM Cho, AC DeVries, JR Williams, CS Carter, The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113, 1071–1079 (1999).
4
TR Insel, ZX Wang, CF Ferris, Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14, 5381–5392 (1994).
5
AG Ophir, JO Wolff, SM Phelps, Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc Natl Acad Sci USA 105, 1249–1254 (2008).
6
MM Lim, et al., Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754–757 (2004).
7
LJ Young, et al., Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400, 766–768 (1999).
8
EA Hammock, LJ Young, Variation in the vasopressin V1a receptor promoter and expression: Implications for inter- and intraspecific variation in social behaviour. Eur J Neurosci 16, 399–402 (2002).
9
M Thibonnier, et al., Structure, sequence, expression, and chromosomal localization of the human V1a vasopressin receptor gene. Genomics 31, 327–334 (1996).
10
M Thibonnier, et al., Study of V(1)-vascular vasopressin receptor gene microsatellite polymorphisms in human essential hypertension. J Mol Cell Cardiol 32, 557–564 (2000).
11
SJ Kim, et al., Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol Psychiatry 7, 503–507 (2002).
12
TH Wassink, et al., Examination of AVPR1a as an autism susceptibility gene. Mol Psychiatry 9, 968–972 (2004).
13
N Yirmiya, et al., Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: Mediation by socialization skills. Mol Psychiatry 11, 488–494 (2006).
14
ZM Prichard, AJ Mackinnon, AF Jorm, S Easteal, AVPR1A and OXTR polymorphisms are associated with sexual and reproductive behavioral phenotypes in humans. Mutation in brief no. 981 Online Hum Mutat 28, 1150 (2007).
15
A Knafo, et al., Individual differences in allocation of funds in the dictator game associated with length of the arginine vasopressin 1a receptor RS3 promoter region and correlation between RS3 length and hippocampal mRNA. Genes Brain Behav 7, 266–275 (2007).
16
JM Neiderhiser, et al., Father-adolescent relationships and the role of genotype-environment correlation. J Fam Psychol 21, 560–571 (2007).
17
A Meyer-Lindenberg, et al., Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol Psychiatry, epub ahead of print. (2008).
18
TH Holmes, RH Rahe, The Social Readjustment Rating Scale. J Psychosomatic Res 11, 213–218 (1967).
19
GB Spanier, Measuring Dyadic Adjustment: New scales for Assessing the Quality of Marriage and Similar Dyads. J Marr Fam 38, 15–28 (1976).
20
JT Winslow, et al., A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545–548 (1993).
21
A Fuentes, Patterns and Trends in Primate Pair Bonds. Internat J Primatol 23, 1573–8604 (2002).
22
JR Krebs, NB Davies Behavioral Ecology (Blackwell, London, 1997).
23
A Fuentes, Hylobatid communities: Changing views on pair bonding and social organization in hominoids. Am J Phys Anthropol 43, 33–60 (2000).
24
RA Hinde Primate Social Relationships: An Integrated Approach (Blackwell, Oxford, 1983).
25
DR Rasmussen, Pair-bond strength and stability and reproductive success. Psycholog Rev 88, 274–290 (1981).
26
JA Simpson, Influence of attachment styles on romantic relationships. J Person Soc Psychol 59, 971–980 (1990).
27
A Booth, D Johnson, JN Edwards, Measuring Marital Instability. J Marr Fam 45, 387–394 (1983).
28
DS Falconer, TF Mackay Introduction to Quantitative Genetics (Longman, Harlow, 1996).
29
EL Spotts, et al., Genetic and environmental influences on marital relationships. J Fam Psychol 18, 107–119 (2004).
30
V Jockin, M McGue, DT Lykken, Personality and divorce: A genetic analysis. J Pers Soc Psychol 71, 288–299 (1996).
31
The GLIMMIX Procedure (Sas Institute, Cary, NCAvailable from http://supportsas.com/rnd/app/da/glimmix.html. (2006).
32
SAS/STAT Software (Version 9.1.3) (SAS Institute, Cary, NC, 2007).

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Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 105 | No. 37
September 16, 2008
PubMed: 18765804

Classifications

Submission history

Received: March 28, 2008
Published online: September 16, 2008
Published in issue: September 16, 2008

Keywords

  1. monogamy
  2. neuropeptide
  3. polymorphism
  4. social behavior

Acknowledgments

This project was supported by National Institute of Mental Health Grant R01MH54610, Bank of Sweden Tercentenary Foundation Grant J2004–0036:1, and a postdoctoral fellowship sponsored by the Brain Foundation, Sweden (to L.W.).

Notes

This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0803081105/DCSupplemental.

Authors

Affiliations

Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Box 281, S-171 77 Stockholm, Sweden;
Lars Westberg
Department of Pharmacology, Institute of Neuroscience and Physiology, University of Gothenburg, Box 431, S 405 30 Gothenburg, Sweden;
Susanne Henningsson
Department of Pharmacology, Institute of Neuroscience and Physiology, University of Gothenburg, Box 431, S 405 30 Gothenburg, Sweden;
Jenae M. Neiderhiser
Department of Psychology, Pennsylvania State University, University Park, PA 16802;
David Reiss
Yale Child Study Center, Yale University, New Haven, CT 06520;
Wilmar Igl
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Box 281, S-171 77 Stockholm, Sweden;
Jody M. Ganiban
Department of Psychology, The George Washington University, Building GG 2125 G St NW, Washington, DC 20052; and
Erica L. Spotts
Behavioral and Social Research Program, National Institute on Aging, Bethesda, MD 20892-9205
Nancy L. Pedersen
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Box 281, S-171 77 Stockholm, Sweden;
Elias Eriksson
Department of Pharmacology, Institute of Neuroscience and Physiology, University of Gothenburg, Box 431, S 405 30 Gothenburg, Sweden;
Paul Lichtenstein
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Box 281, S-171 77 Stockholm, Sweden;

Notes

To whom correspondence should be addressed. E-mail: [email protected]
Author contributions: H.W., L.W., S.H., J.M.N., D.R., J.M.G., E.L.S., N.L.P., E.E., and P.L. designed research; W.I. contributed new reagents/analytic tools; H.W. analyzed data; and H.W. and L.W. wrote the paper.
H.W. and L.W. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans
    Proceedings of the National Academy of Sciences
    • Vol. 105
    • No. 37
    • pp. 13697-14234

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