Mammalian monogamy is not controlled by a single gene
Open accessAbstract
Complex social behavior in Microtus voles and other mammals has been postulated to be under the direct genetic control of a single locus: the arginine vasopressin 1a receptor (avpr1a) gene. Using a phylogenetic approach, we show that a repetitive element in the promoter region of avpr1a, which reportedly causes social monogamy, is actually widespread in nonmonogamous Microtus and other rodents. There was no evidence for intraspecific polymorphism in regard to the presence or absence of the repetitive element. Among 25 rodent species studied, the element was absent in only two closely related nonmonogamous species, indicating that this absence is certainly the result of an evolutionarily recent loss. Our analyses further demonstrate that the repetitive structures upstream of the avpr1a gene in humans and primates, which have been associated with social bonding, are evolutionarily distinct from those in rodents. Our evolutionary approach reveals that monogamy in rodents is not controlled by a single polymorphism in the promoter region of the avpr1a gene. We thus resolve the contradiction between the claims for an evolutionarily conserved genetic programming of social behavior in mammals and the vast evidence for highly complex and flexible mating systems.
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Length per se does not predict social organization of other Microtus species.
“However, it is now known that length per se does not predict social organization of other Microtus species [29, 32], and sequence variation within the microsatellite may have a greater influence on expression than length itself [3].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [32]
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Beyond Neuroanatomy: Novel Approaches to Studying Brain Evolution
Pollen, A. A., & Hofmann, H. A. (2008) · Brain Behavior and Evolution · doi:10.1159/000151474 · Cited by 34 · see citing works
“However, it should be noted that the presence or absence of this expanded microsatellite repeat does not correlate with the mating systems in other Microtus vole species [Fink et al., 2006].”
BackgroundPair bonds and parental behaviour
McGraw, L. A., Székely, T., & Young, L. J. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511781360.023 · Cited by 37 · see citing works
Tecot, S. R., & Baden, A. L. (2015) · Emerging Trends in the Social and Behavioral Sciences · doi:10.1002/9781118900772.etrds0263 · Cited by 36 · see citing works
Systematics of snow voles (Chionomys, Arvicolinae) revisited.
Yannic, G., Burri, R., Malikov, V., & Vogel, P. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.12.004 · Cited by 34 · see citing works
Chimpanzee Personality and the Arginine Vasopressin Receptor 1A Genotype
Wilson, V. A. D., Weiss, A., Humle, T., Morimura, N., Udono, T., Idani, G., Matsuzawa, T., Hirata, S., & Inoue‐Murayama, M. (2016) · Behavior Genetics · doi:10.1007/s10519-016-9822-2 · Cited by 32 · see citing works
“However, further analyses of AVPR1a across 21 Microtus species did not find an association between partner preferences and the AVPR1a genotype (Fink et al. 2006).”
BackgroundSadino, J. M., & Donaldson, Z. R. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00475 · Cited by 28 · see citing works
Fitness, risk taking, and spatial behavior covary with boldness in experimental vole populations
Eccard, J. A., Herde, A., Schuster, A., Liesenjohann, T., Knopp, T., Heckel, G., & Dammhahn, M. (2022) · Ecology and Evolution · doi:10.1002/ece3.8521 · Cited by 30 · see citing works
“…characterized by a high reproductive potential balancing strong predation pressure, a promiscuous mating system (Borkowska & Ratkiewicz, 2010; Fink et al., 2006), larger home ranges of males than females (as other Microtus species: Borowski & Owadowska, 2010; Gliwicz, 1997; Solomon &…”
BackgroundMacManes, M. D., & Lacey, E. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045524 · Cited by 29 · see citing works
“This strategy has been used to explore differences in gene expression in relation to multiple aspects of behavior, including the formation of social bonds [18–20].”
MethodBabb, P. L., Fernández‐Duque, E., & Schurr, T. G. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9383-6 · Cited by 29 · see citing works
“These findings coincide with levels of intraspecific sequence diversity observed in other studies of the AVPR1A coding region in mammalian taxa (Fink et al. 2006, 2007; Phelps et al. 2009; Turner et al. 2010).”
BackgroundResultInfluentialAnestis, S. F., Webster, T. H., Kamilar, J. M., Fontenot, M. B., Watts, D. P., & Bradley, B. J. (2014) · International Journal of Primatology · doi:10.1007/s10764-013-9747-z · Cited by 29 · see citing works
“…B. Fontenot Behavioral Sciences Division, New Iberia Research Center, University of Louisiana, Lafayette, LA 70562, USA we had quantitative measures of personality (based on 15 behavioral style indices, calculated from 3 yr of observational data), dominance rank, and baseline testosterone levels.”
BackgroundMethodRen, D., Chin, K. R., & French, J. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111638 · Cited by 28 · see citing works
“is not predicted by a single polymorphism in the promoter region of the AVPR1a gene [12].”
BackgroundManinger, N., Hinde, K., Mendoza, S. P., Mason, W. A., Larke, R. H., Ragen, B., Jarcho, M. R., Cherry, S. R., Rowland, D. J., Ferrer, E. E., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.02.028 · Cited by 27 · see citing works
“However, this pattern was not found across a wider sample of mammalian species (Fink et al., 2006).”
Ophir, A. G., Crino, O. L., Wilkerson-Vidal, Q. C., Wolff, J. O., & Phelps, S. M. (2007) · Brain Behavior and Evolution · doi:10.1159/000108609 · Cited by 26 · see citing works
“Allelic diversity in the genetic architecture of the V1aR coding sequence may further complicate the story [Hammock and Young, 2005; Fink et al., 2006].”
BackgroundSex-specific clines support incipient speciation in a common European mammal
Sutter, A., Beysard, M., & Heckel, G. (2013) · Heredity · doi:10.1038/hdy.2012.124 · Cited by 26 · see citing works
Gene Regulation as a Modulator of Social Preference in Voles
Hammock, E. A. D. (2007) · Advances in genetics · doi:10.1016/s0065-2660(07)59004-8 · Cited by 26 · see citing works
Microsatellite markers for the common vole (Microtus arvalis) and their cross-species utility
Walser, B., & Heckel, G. (2007) · Conservation Genetics · doi:10.1007/s10592-007-9355-6 · Cited by 26 · see citing works
“The markers are currently being employed in studies of dispersal and reproductive success in natural and experimental populations (Fink et al. 2006).”
BackgroundEvolutionary diversity as a catalyst for biological discovery
JOHNSON, Z. V., & YOUNG, L. J. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12339 · Cited by 25 · see citing works
Cushing, B. S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150373 · Cited by 25 · see citing works
“However this relationship does not exist in many other rodent taxa, and in fact it has been observed that outside the genus Microtus there is no correlation between microsatellite length and mating strategy [56].”
BackgroundBeysard, M., Krebs-Wheaton, R., & Heckel, G. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0455-5 · Cited by 25 · see citing works
“Given the polygynous mating system of the common vole with frequent multiple paternity [46, 47], the influence of mate choice of female M.”
BackgroundRhodes, J. S., & Kawecki, T. J. (2009) · University of California Press eBooks · doi:10.1525/california/9780520247666.003.0011 · Cited by 23 · see citing works
“Despite all the positive evidence, a recent phylogenetic analysis failed to find the predicted association between expansion in this microsatellite region and affiliative behavior in a larger sample of twenty-three species of voles (Fink et al. 2006).”
BackgroundFrom endophenotypes to evolution: social attachment, sexual fidelity and the avpr1a locus
Phelps, S. M. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.09.002 · Cited by 23 · see citing works
“[39] found that the promiscuous montane and meadow voles lacked the microsatellite, as previously reported, but the other 4 Microtus species known to be promiscuous all had long microsatellites.”
BackgroundVasopressin Proves Essential: Vasopressin and the Modulation of Sensory Processing in Mammals
Bester‐Meredith, J. K., Fancher, A. P., & Mammarella, G. E. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00005 · Cited by 23 · see citing works
Towards an integrative model of sociality in caviomorph rodents
Hayes, L. D., Burger, J. R., Soto-Gamboa, M. R., Sobrero, R., & Ebensperger, L. A. (2011) · Journal of Mammalogy · doi:10.1644/10-mamm-s-039.1 · Cited by 21 · see citing works
“Towards an integrative model of sociality in caviomorph rodents”
BackgroundGlobal Microsatellite Content Distinguishes Humans, Primates, Animals, and Plants
Galindo, C. L., McIver, L. J., McCormick, J. F., Skinner, M. A., Xie, Y., Gelhausen, R., Ng, K.-M. E., Kumar, N., & Garner, H. R. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp192 · Cited by 21 · see citing works
“This is the first description of a method for evaluating microsatellite content to classify individual genomes.”
BackgroundMethodOxytocin, vasopressin, and the evolution of mating systems in mammals
Freeman, S. M., & Young, L. J. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.011 · Cited by 19 · see citing works
Voles, vasopressin, and infidelity: a molecular basis for monogamy, a platform for ethics, and more?
McKaughan, D. J. (2011) · Biology & Philosophy · doi:10.1007/s10539-011-9303-1 · Cited by 19 · see citing works
“Not only do these results cast doubt on the claim that a single gene, V1aR, controls monogamy in any straightforward way, reconstruction of the phylogenetic relationships (based on comparative cytochrome b sequencing) demonstrate that the longer microsatellites (STRs) are actually the ancestral state in voles (Fink et…”
BackgroundResultFreeman, A. R., Aulino, E. A., Caldwell, H. K., & Ophir, A. G. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12828 · Cited by 19 · see citing works
Tougard, C. (2016) · Journal of Zoological Systematics & Evolutionary Research · doi:10.1111/jzs.12152 · Cited by 19 · see citing works
“…AY513842 AY513844 JN019765 JN019766 JN019773 JN019775 JN019778 JN019780 JN019762 JN019763 AY513840 JN019760 JN019761 JN019767 JN019764 JN019768 JN019771 NM H E E H H H H H H H H E H H H H H H a A: Bastos-Silveira et al. (2012); B: Castiglia et al. (2008); C: Fink et al. (2006); D: Haynes et 1 al.”
Borkowska, A., & Ratkiewicz, M. (2010) · Journal of Zoology · doi:10.1111/j.1469-7998.2009.00648.x · Cited by 19 · see citing works
Stetzik, L. A., Ganshevsky, D., Lende, M. N., Roache, L. E., Musatov, S. A., & Cushing, B. S. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.035 · Cited by 18 · see citing works
“Based upon the hypothesis that multiple mechanisms regulate social behavior [45], specifically involving an interaction between steroids and the neuropeptides oxytocin and vasopressin [4,34,46], the intermediate expression of ERα may explain why, like prairie voles, but unlike montane voles, central administration of…”
The neuroendocrine action potential
Hofmann, H. A. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.012 · Cited by 18 · see citing works
“A comparative analysis of PEI across the genus Microtuswould be worthwhile, as some species are (either genetically or socially) monogamous and others are polygamous (Fink et al., 2006).”
BackgroundInfluentialOxytocin and vasopressin in non-human primates
Ragen, B., & Bales, K. L. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.019 · Cited by 18 · see citing works
Modulating vertebrate physiology by genomic fine-tuning of GPCR functions
Schöneberg, T. (2024) · Physiological Reviews · doi:10.1152/physrev.00017.2024 · Cited by 17 · see citing works
Multiple paternity in free-living root voles (Microtus oeconomus)
Borkowska, A., Borowski, Z., & Krysiuk, K. (2009) · Behavioural Processes · doi:10.1016/j.beproc.2009.05.003 · Cited by 17 · see citing works
On the origins of diversity in social behavior
YOUNG, L. J., & ZHANG, Q. (2021) · Japanese Journal of Animal Psychology · doi:10.2502/janip.71.1.4 · Cited by 13 · see citing works
Evolution of the arginine vasopressin 1a receptor and implications for mammalian social behaviour
Heckel, G., & FINK, S. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00426-3 · Cited by 13 · see citing works
From biology to management of Savi's pine vole (Microtus savii)
Ranchelli, E., Barfknecht, R., Capizzi, D., Riga, F., Mazza, V., Dell’Agnello, F., & Zaccaroni, M. (2015) · Pest Management Science · doi:10.1002/ps.4212 · Cited by 13 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00004-3 · Cited by 13 · see citing works
Has Simple Sequence Repeat Mutability Been Selected to Facilitate Evolution?
Kashia, Y., & King, D. G. (2006) · Israel Journal of Ecology and Evolution · doi:10.1560/ijee_52_3-4_331 · Cited by 13 · see citing works
Mate Selection, Sexual Orientation, and Pair Bonding
Balthazart, J., & Young, L. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00048-x · Cited by 12 · see citing works
The neural circuits of monogamous behavior
López-Gutiérrez, M. F., Mejía-Chávez, S., Alcauter, S., & Portillo, W. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.978344 · Cited by 11 · see citing works
“Hence, the complexity of social monogamy has led to the conclusion that no single gene, brain structure, or neurotransmitter system can be the sole modulator of the observed behaviors (Fink et al., 2006).”
BackgroundKeane, B., Parsons, S., Smucker, B. J., & Solomon, N. G. (2014) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-014-1801-0 · Cited by 11 · see citing works
The Neurobiology and Genetics of Affiliation and Social Bonding in Animal Models
Donaldson, Z. R., & Young, L. J. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3777-6_4 · Cited by 11 · see citing works
Phylogeny and phylogeography of arvicoline and lagurine voles of Mongolia
Bannikova, A. A., Lebedev, V. S., Poplavskaya, N. S., Simanovsky, S. A., Undrakhbayar, E., Adiya, Y., & Суров, А. В. (2019) · Folia Zoologica · doi:10.25225/fozo.002.2019 · Cited by 11 · see citing works
Henterly, A. C., Mabry, K. E., Solomon, N. G., Chesh, A. S., & Keane, B. (2011) · The American Midland Naturalist · doi:10.1674/0003-0031-165.2.412 · Cited by 9 · see citing works
“…species-specific genetic polymorphism in avpr1a allele length between Microtus ochrogaster and M. pennsylvanicus, with M. ochrogaster containing an expanded segment of repetitive microsatellite DNA in the avpr1a gene that is absent in M. pennsylvanicus (Young et al., 1999; Fink et al., 2006).”
BackgroundInfluentialPost‐fertilization Reproductive Strategies
van Dijk, R. E., & Székely, T. (2008) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0003665 · Cited by 9 · see citing works
“Studies beyond these well-studied voles, however, in other species of voles and in primates found no consistent relationship between microsatellite length and mating system (Fink et al., 2006).”
BackgroundComparative neurobiology and genetics of mammalian social behavior
Beery, A. K., Kamal, Y., Sobrero, R., & Hayes, L. D. (2016) · Wiley eBooks · doi:10.1002/9781118846506.ch3 · Cited by 9 · see citing works
Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field
Lambert, C. T., Lichter, J. B., Perry, A. N., Castillo, S. A., Keane, B., Cushing, B. S., & Solomon, N. G. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0318 · Cited by 7 · see citing works
“Although laboratory studies have indicated a major influence of AVP, attempts to translate these studies to other socially monogamous mammals [26] or field settings have either not produced the predicted results or produced conflicting results [27–33].”
ResultRethinking the Architecture of Attachment: New Insights into the Role for Oxytocin Signaling
Berendzen, K. M., & Manoli, D. S. (2022) · Affective Science · doi:10.1007/s42761-022-00142-5 · Cited by 9 · see citing works
“Numerous reviews and studies over the last decade have expressed caution in attributing widespread, functional necessity to oxytocinergic signaling in social behavior (Fink et al., 2006; Goodson, 2013; Guastella & Hickie, 2016).”
BackgroundAdvancing avian behavioral neuroendocrinology through genomics
Clayton, D. F., & London, S. E. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.09.004 · Cited by 7 · see citing works
“EventhecaseoftheV1areceptorpolymorphismismorecom- plexthaninitialreportsimplied,asaphylogeneticanalysisof25 rodentspeciesfailedtoconfirmtheassociationofthisparticular polymorphismwithsocialmonogamymorebroadly(Fink,2006).”
Anderson, N. K., Goodwin, S. E., Schuppe, E. R., Dawn, A., Preininger, D., Mangiamele, L. A., & Fuxjager, M. J. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105248 · Cited by 7 · see citing works
Social Games and Genic Selection Drive Mammalian Mating System Evolution and Speciation
Sinervo, B., Chaine, A. S., & Miles, D. B. (2019) · The American Naturalist · doi:10.1086/706810 · Cited by 7 · see citing works
“…monogamy and polygyny in rodents have been linked to a point mutation in a vasopressin receptor gene (V1aR; Lim and Young 2004; Lim et al. 2004; Fink et al. 2006), and this gene is also linked to increased paternal behavior and reduced aggression (i.e., filiative behavior) inmonogamous species…”
Background
- Authors
- Fink, S., Excoffier, L., & Heckel, G.
- Affiliations
- University of Bern (CH)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-07-18
- Volume
- 103
- Issue
- 29
- Pages
- 10956-10960
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1544156
- OpenAlex
- W2012695658
- Cited by
- 133
- References
- 40
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2022: 6 · 2021: 3 · 2020: 2 · 2019: 5 · 2018: 4 · 2017: 2 · 2016: 12 · 2015: 10 · 2014: 9 · 2013: 10 · 2012: 6
- FWCI
- 18.07
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- BORIS (University Library Bern) (submittedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Keywords
- social monogamy, Microtus voles, social behavior genetics, gene loss, social bonding
- MeSH terms
- Animals, Humans, Molecular Sequence Data, Phylogeny, Rodentia, Sexual Behavior, Animal, Social Behavior, Receptors, Vasopressin, Cytochromes b
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