The DOI matches its Crossref record; 28 of the 29 references it cites were found in a registry or an index.
Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene.
Abstract
The molecular mechanisms underlying the evolution of complex behaviour are poorly understood. The mammalian genus Microtus provides an excellent model for investigating the evolution of social behaviour. Prairie voles (Microtus ochrogaster) exhibit a monogamous social structure in nature, whereas closely related meadow voles (Microtus pennsylvanicus) are solitary and polygamous. In male prairie voles, both vasopressin and dopamine act in the ventral forebrain to regulate selective affiliation between adult mates, known as pair bond formation, as assessed by partner preference in the laboratory. The vasopressin V1a receptor (V1aR) is expressed at higher levels in the ventral forebrain of monogamous than in promiscuous vole species, whereas dopamine receptor distribution is relatively conserved between species. Here we substantially increase partner preference formation in the socially promiscuous meadow vole by using viral vector V1aR gene transfer into the ventral forebrain. We show that a change in the expression of a single gene in the larger context of pre-existing genetic and neural circuits can profoundly alter social behaviour, providing a potential molecular mechanism for the rapid evolution of complex social behaviour.
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In the citing paper
“While achieving relationship satisfaction is a primary goal for most individuals, only 37% of couples claim to be very happy in their marriage [24].”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [24]
In the citing paper
“Pair-bonded prairie voles spend more time with their partner than with the stranger, whereas non-monogamous meadow voles (Microtus pennsylvanicus) spend little time interacting with their partner or stranger [138].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [138]
In the citing paper
“Conversely, viral-mediated increases in VP AVPR1a expression induce partner preferences and increase affiliative behaviors in male prairie voles that are sexually naïve and, interestingly, also lead to partner preference formation in non-monogamous meadow voles [138,146].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [138]
In the citing paper
“Over-expressing the gene encoding the prairie vole AVPR1A, Avpr1a, in the ventral pallidum of male meadow voles using viral vector-mediated gene transfer results in the ability of this promiscuous species to display partner preferences [23].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [23]
In the citing paper
“Viral-mediated Avpr1a receptor overexpression studies show that species differences in Avpr1a expression mediate species differences in social behavior, and variation in Avpr1a expression in the brain is related to microsatellite diversity in the gene's 5′ flanking region (151-154).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [152]
Citations
Cites
Kleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 1×
“Central administration of vasopressin facilitates each of these monogamous-typical behaviours in male prairie voles through V1aRs in the brai”
BackgroundBielsky, I. F., Hu, S.-B., Szegda, K. L., Westphal, H., & Young, L. J. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300360 · Cited by 531
Self-citationYoung, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R., & Insel, T. R. (1999) · Nature · doi:10.1038/23475 · Cited by 488
Self-citationInsel, T., Wang, Z., & Ferris, C. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05381.1994 · Cited by 454
Self-citationVasopressin and oxytocin receptors in the central nervous system
Tribollet, E., & Barberis, C. (1996) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v10.i1.60 · Cited by 399
Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
Wang, Z., Ferris, C. F., & De Vries, G. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.400 · Cited by 381
Self-citationA critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles
Aragona, B. J., Liu, Y., Curtis, J. T., Stephan, F. K., & Wang, Z. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03483.2003 · Cited by 351
Self-citationGingrich, B., Liu, Y., Cascio, C., Wang, Z., & Insel, T. R. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.1.173 · Cited by 339
Self-citationVasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole
Lim, M. M., & Young, L. J. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.008 · Cited by 322
Self-citationPitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07392.2001 · Cited by 295
Self-citationBester‐Meredith, J. K., Young, L. J., & Marler, C. A. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1522 · Cited by 285
Self-citationKim, S.-J., Young, L. J., Gonen, D., Veenstra-VanderWeele, J., Courchesne, R., Courchesne, E., Lord, C., Leventhal, B. L., Cook Jr, E. H., & Insel, T. R. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001125 · Cited by 265
Self-citationOxytocin and Vasopressin Receptors and Species-Typical Social Behaviors
Young, L. J. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1548 · Cited by 211
Self-citationWang, Z., Yu, G., Cascio, C., Liu, Y., Gingrich, B., & Insel, T. R. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.3.602 · Cited by 205
Self-citationYoung, L. J., Winslow, J. T., Nilsen, R., & Insel, T. R. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.3.599 · Cited by 196
Self-citationLandgraf, R., Frank, E., Aldag, J. M., Neumann, I. D., Sharer, C. A., Ren, X., Terwilliger, E. F., Niwa, M., Wigger, A., & Young, L. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02750.x · Cited by 169
Self-citationLim, M. M., Murphy, A. Z., & Young, L. J. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10973 · Cited by 163
Self-citationCooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation
Roberts, R. L., WILLIAMS, J. R., Wang, A. S., & Carter, C. S. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0659 · Cited by 152
Comparison of the Mating System and Paternal Behavior in Microtus ochrogaster and M. pennsylvanicus
Gruder-Adams, S., & Getz, L. L. (1985) · Journal of Mammalogy · doi:10.2307/1380976 · Cited by 142
Localization of Vasopressin (V1a) Receptor Binding and mRNA in the Rhesus Monkey Brain
Young, Toloczko, & Insel (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00332.x · Cited by 139
Functional Microsatellite Polymorphism Associated with Divergent Social Structure in Vole Species
Hammock, E. A. D. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh104 · Cited by 122
Phelps, S. M., & Young, L. J. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10902 · Cited by 116
Self-citationSocial behavior and comparative genomics: new genes or new gene regulation?
Robinson, G. E., & Ben‐Shahar, Y. (2002) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2002.10401.x · Cited by 101
Hammock, E. A. D., & Young, L. J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02083.x · Cited by 95
Self-citationWang, Z., Toloczko, D., Young, L. J., Moody, K., Newman, J. D., & Insel, T. R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00636-7 · Cited by 75
Self-citationBehavioral Consequences of Trauma
Gensemer, I. B., McMurry, F. G., WALKER, J. C., Monasky, M., & BROTMAN, S. J. (1988) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-198801000-00006 · Cited by 64
Parker, K. J., Phillips, K. M., & Lee, T. M. (2001) · Animal Behaviour · doi:10.1006/anbe.2000.1707 · Cited by 41
Research works printed but not linked: 1
- Aragona, B. J. et al. Opposite modulation of social attachment by D1- and D2-type dopamine receptor activation in nucleus accumbens shell. Horm. Behav. 44, 37 (2003)
Cited by
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Oxytocin, vasopressin, and the neurogenetics of sociality
Donaldson, Z. R., & Young, L. J. (2008) · Science · doi:10.1126/science.1158668 · Cited by 1,645
Self-citationThe neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523
Self-citationBehavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462
Neural reuse: A fundamental organizational principle of the brain
Anderson, M. L. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x10000853 · Cited by 1,212
Fonagy, P., & Luyten, P. (2009) · Development and Psychopathology · doi:10.1017/s0954579409990198 · Cited by 1,146
“pecially in males (Caldwell, Lee, Macbeth, & Young, 2008; Lim et al., 2004).”
Background
Metadata
- Authors
- Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J.
- Affiliations
- Emory University (US)
- Florida State University (US)
- Beth Israel Deaconess Medical Center (US)
- Corresponding author
- Young, Larry J.
- Venue
- Nature
- Published
- 2004-06
- Volume
- 429
- Issue
- 6993
- Pages
- 754-757
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2022927508
- Cited by
- 628
- References
- 29
- Citations by year
- 2026: 19 · 2025: 20 · 2024: 17 · 2023: 17 · 2022: 42 · 2021: 18 · 2020: 18 · 2019: 15 · 2018: 24 · 2017: 27 · 2016: 28 · 2015: 24 · 2014: 32 · 2013: 29 · 2012: 33
- FWCI
- 58.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- mate preferences, pair bonding, vasopressin V1a receptor, Microtus pennsylvanicus, Microtus ochrogaster, Microtus, evolution of social behavior, ventral forebrain, dopamine, viral gene delivery, monogamy, polygamy, promiscuity
- MeSH terms
- Animals, Choice Behavior, Arvicolinae, Female, Male, Pair Bond, Receptors, Dopamine, Sexual Behavior, Animal, Prosencephalon, Receptors, Vasopressin
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