Facial shape differences between rats selected for tame and aggressive behaviors
Open accessAbstract
Domestication has been consistently accompanied by a suite of traits called the domestication syndrome. These include increased docility, changes in coat coloration, prolonged juvenile behaviors, modified function of adrenal glands and reduced craniofacial dimensions. Wilkins et al recently proposed that the mechanistic factor underlying traits that encompass the domestication syndrome was altered neural crest cell (NCC) development. NCC form the precursors to a large number of tissue types including pigment cells, adrenal glands, teeth and the bones of the face. The hypothesis that deficits in NCC development can account for the domestication syndrome was partly based on the outcomes of Dmitri Belyaev's domestication experiments initially conducted on silver foxes. After generations of selecting for tameness, the foxes displayed phenotypes observed in domesticated species. Belyaev also had a colony of rats selected over 64 generations for either tameness or defensive aggression towards humans. Here we focus on the facial morphology of Belyaev's tame, 'domesticated' rats to test whether: 1) tameness in rats causes craniofacial changes similar to those observed in the foxes; 2) facial shape, i.e. NCC-derived region, is distinct in the tame and aggressive rats. We used computed-tomography scans of rat skulls and landmark-based geometric morphometrics to quantify and analyze the facial skeleton. We found facial shape differences between the tame and aggressive rats that were independent of size and which mirrored changes seen in domesticated animals compared to their wild counterparts. However, there was no evidence of reduced sexual dimorphism in the face of the tame rats. This indicates that not all morphological changes in NCC-derived regions in the rats follow the pattern of shape change reported in domesticated animals or the silver foxes. Thus, certain phenotypic trends that are part of the domestication syndrome might not be consistently present in all experimental animal models.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Selection for tameness is enough to bring about a constellation of domestic traits, many of which humans share.
“Crucially, this suggests that selection for tameness is enough to bring about a constellation of domestic traits (see [33]), many of which humans share.”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [33]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Morpho J: an integrated software package for geometric morphometrics
Klingenberg, C. P. (2010) · Molecular Ecology Resources · doi:10.1111/j.1755-0998.2010.02924.x · Cited by 3,784 · see citing works
Statistical shape analysis: clustering, learning, and testing
Srivastava, A., Joshi, S. K., Mio, W., & Liu, X. (2005) · IEEE Transactions on Pattern Analysis and Machine Intelligence · doi:10.1109/tpami.2005.86 · Cited by 2,728 · see citing works
Ornitz, D. M., & Itoh, N. (2001) · Genome biology · doi:10.1186/gb-2001-2-3-reviews3005 · Cited by 1,985 · see citing works
Fibroblast growth factors, their receptors and signaling
Powers, C. J., McLeskey, S. W., & Wellstein, A. (2000) · Endocrine-related cancer · doi:10.1677/erc.0.0070165 · Cited by 1,332 · see citing works
Wilkins, A. S., Wrangham, R. W., & Fitch, W. T. (2014) · Genetics · doi:10.1534/genetics.114.165423 · Cited by 751 · see citing works
Animal evolution during domestication: the domesticated fox as a model
Trut, L., Oskina, I., & Kharlamova, A. (2009) · BioEssays · doi:10.1002/bies.200800070 · Cited by 636 · see citing works
Self-citationEarly canid domestication: the farm-fox experiment.
Trut, L. (1999) · American Scientist · doi:10.1511/1999.2.160 · Cited by 626 · see citing works
Self-citationHare, B., Wobber, V., & Wrangham, R. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2011.12.007 · Cited by 613 · see citing works
Corticosteroids in relation to fear, anxiety and psychopathology
Korte, S. M. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00002-1 · Cited by 607 · see citing works
Dai, M., Kurtek, S., Klassen, E. P., et al. (2021) · Springer eBooks · doi:10.1007/978-3-030-63416-2_778 · Cited by 418 · see citing works
Antenatal Glucocorticoids and Programming of the Developing CNS
Matthews, S. G. (2000) · Pediatric Research · doi:10.1203/00006450-200003000-00003 · Cited by 400 · see citing works
Dryden, I. L., & Mardia, K. V. (1998) · Cited by 388 · see citing works
Cell lineage in mammalian craniofacial mesenchyme.
Yoshida, T., Vivatbutsiri, P., Morriss-Kay, G., Saga, Y., & Iseki, S. (2008) · Mechanisms of Development · doi:10.1016/j.mod.2008.06.007 · Cited by 384 · see citing works
Social Cognitive Evolution in Captive Foxes Is a Correlated By-Product of Experimental Domestication
Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., & Trut, L. (2005) · Current Biology · doi:10.1016/j.cub.2005.01.040 · Cited by 347 · see citing works
Self-citationOrigins of the dog: domestication and early history
Clutton–Brock, J. (1995) · Cited by 327 · see citing works
Development and tissue origins of the mammalian cranial base
McBratney‐Owen, B., Iseki, S., Bamforth, S. D., Olsen, B. R., & Morriss‐Kay, G. M. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.07.016 · Cited by 296 · see citing works
CRANIAL MORPHOLOGY OF DOMESTIC AND WILD CANIDS: THE INFLUENCE OF DEVELOPMENT ON MORPHOLOGICAL CHANGE
Wayne, R. K. (1986) · Evolution · doi:10.1111/j.1558-5646.1986.tb00467.x · Cited by 271 · see citing works
The effects of captivity on the morphology of captive, domesticated and feral mammals
O’Regan, H. J., & Kitchener, A. C. (2005) · Mammal Review · doi:10.1111/j.1365-2907.2005.00070.x · Cited by 264 · see citing works
The role of behavior in evolution: a search for mechanism
Duckworth, R. A. (2008) · Evolutionary Ecology · doi:10.1007/s10682-008-9252-6 · Cited by 258 · see citing works
The early evolution of the domestic dog
Morey, D. F. (1994) · American Scientist · Cited by 227 · see citing works
Paedomorphic Facial Expressions Give Dogs a Selective Advantage
Waller, B. M., Peirce, K., Caeiro, C. C., Scheider, L., Burrows, A. M., McCune, S., & Kaminski, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082686 · Cited by 214 · see citing works
An Experiment on Fox Domestication and Debatable Issues of Evolution of the Dog
Trut, L. N., Plyusnina, I. Z., & Oskina, I. N. (2004) · Russian Journal of Genetics · doi:10.1023/b:ruge.0000033312.92773.c1 · Cited by 197 · see citing works
Self-citationSánchez-Villagra, M. R., Geiger, M., & Schneider, R. A. (2016) · Royal Society Open Science · doi:10.1098/rsos.160107 · Cited by 195 · see citing works
Dogs : A New Understanding of Canine Origin, Behavior and Evolution
Coppinger, L., & Coppinger, R. (2001) · Cited by 175 · see citing works
Belyaev, D. K., Plyusnina, I. Z., & Trut, L. N. (1985) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(85)90015-2 · Cited by 173 · see citing works
Self-citationAlbert, F. W., Shchepina, O., Winter, C., Römpler, H., Teupser, D., Palme, R., Ceglarek, U., Kratzsch, J., Sohr, R., Trut, L. N., et al. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.11.010 · Cited by 157 · see citing works
Self-citationMurrin, L. C., Sanders, J. D., & Bylund, D. B. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.01.028 · Cited by 152 · see citing works
Young, N. M., Chong, H. J., Hu, D. P., Hallgrímsson, B., & Marcucio, R. (2010) · Development · doi:10.1242/dev.052340 · Cited by 140 · see citing works
Francis‐West, P. H., Tatla, T. S., & Brickell, P. M. (1994) · Developmental Dynamics · doi:10.1002/aja.1002010207 · Cited by 136 · see citing works
Genetic architecture of tameness in a rat model of animal domestication
Albert, F. W., Carlborg, O., Plyusnina, I., Besnier, F., Hedwig, D., Lautenschläger, S., Lorenz, D., McIntosh, J., Neumann, C., Richter, H., et al. (2009) · Genetics · doi:10.1534/genetics.109.102186 · Cited by 136 · see citing works
Self-citationEmbryonic bauplans and the developmental origins of facial diversity and constraint
Young, N. M., Hu, D. P., Lainoff, A. J., Smith, F. J., Díaz, R. E., Tucker, A. S., Trainor, P. A., Schneider, R. A., Hallgrímsson, B., & Marcucio, R. (2014) · Development · doi:10.1242/dev.099994 · Cited by 130 · see citing works
Evidence for the involvement of central serotonin in mechanism of domestication of silver foxes
Popova, N. K., Voǐtenko, N. N., Kulikov, A. V., & Avgustinovich, D. F. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90080-l · Cited by 128 · see citing works
Cranial Morphology of Domestic and Wild Canids: The Influence of Development on Morphological Change
Wayne, R. K. (1986) · Evolution · doi:10.2307/2408805 · Cited by 122 · see citing works
Drake, A. G. (2011) · Evolution & Development · doi:10.1111/j.1525-142x.2011.00470.x · Cited by 107 · see citing works
Jiang, X., Choudhary, B., Merki, E., Chien, K. R., Maxson, R. E., & Sucov, H. M. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00206-x · Cited by 107 · see citing works
Foppiano, S., Hu, D. P., & Marcucio, R. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.016 · Cited by 98 · see citing works
PLYUSNINA, I., & OSKINA, I. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00445-3 · Cited by 98 · see citing works
Self-citationLord, K. A., Schneider, R. A., & Coppinger, R. (2016) · Cambridge University Press eBooks · doi:10.1017/9781139161800.004 · Cited by 96 · see citing works
It's all in your head: new insights into craniofacial development and deformation
Tapadia, M. D., Cordero, D. R., & Helms, J. A. (2005) · Journal of Anatomy · doi:10.1111/j.1469-7580.2005.00484.x · Cited by 94 · see citing works
Popova, N. K., Kulikov, A. V., Nikulina, E. M., Kozlachkova, E. Y., & Maslova, G. B. (1991) · Aggressive Behavior · doi:10.1002/1098-2337(1991)17:4 · Cited by 79 · see citing works
Trut, L. N. (2016) · Cited by 65 · see citing works
Self-citationMartínez‐Abadías, N., Heuzé, Y., Wang, Y., Jabs, E. W., Aldridge, K. J., & Richtsmeier, J. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026425 · Cited by 61 · see citing works
Bone morphogenetic protein-2 and -4 expression during murine orofacial development
Bennett, J., Hunt, P., & Thorogood, P. (1995) · Archives of Oral Biology · doi:10.1016/0003-9969(95)00047-s · Cited by 56 · see citing works
Effect of Domestication on Aggression in Gray Norway Rats
Plyusnina, I. Z., Solov’eva, M. Y., & Oskina, I. N. (2011) · Behavior Genetics · doi:10.1007/s10519-010-9429-y · Cited by 49 · see citing works
Self-citationAlves, R. R. N. (2016) · Springer eBooks · doi:10.1007/978-3-319-28155-1_32 · Cited by 40 · see citing works
Oltenacu, E. A. B. (2004) · CRC Press eBooks · doi:10.1201/9781482276664-89 · Cited by 37 · see citing works
Consequences of domestication: morphological diversity of the dog.
Wayne, R. K. (2001) · CABI Publishing eBooks · doi:10.1079/9780851995205.0043 · Cited by 34 · see citing works
Regulation of Jaw Length During Development, Disease, and Evolution
Schneider, R. A. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.08.002 · Cited by 25 · see citing works
c-Fos activation and intermale aggression in rats selected for behavior toward humans
Konoshenko, M. Y., Timoshenko, T. V., & Plyusnina, I. Z. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.09.022 · Cited by 20 · see citing works
Self-citation[Intracranial allometry and craniologic changes during domestication of silver foxes].
Ln, T., Dzerzhinskiĭ, F. I., & Vs, N. (1991) · PubMed · Cited by 15 · see citing works
Acute upregulation of hedgehog signaling in mice causes differential effects on cranial morphology
Singh, N., Dutka, T., Devenney, B., et al. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.017889 · Cited by 12 · see citing works
Self-citationSingh, N., Dutka, T., Reeves, R. H., & Richtsmeier, J. T. (2015) · Developmental Dynamics · doi:10.1002/dvdy.24361 · Cited by 9 · see citing works
Self-citationGeo-Morphometric Approaches to the Study of Sexual Size Dimorphism in Murid Rodents
Afshan, K., Rizvi, S. S. R., MUHAMMAD, A. M., et al. (2013) · Pakistan Journal of Zoology · Cited by 2 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [15]Trut N. Canid Domestication: The Farm-Fox Experiment. 2000; Available: http://www.jstor.org/stable/pdf/27857815.pdf
- [19]Slice DE. Modern morphometrics. Modern morphometrics in physical anthropology. Springer; 2005 pp. 1– 45.
Cited by
Sorted by citations
Self-domestication in Homo sapiens: Insights from comparative genomics
Theofanopoulou, C., Gastaldon, S., O’Rourke, T., Samuels, B. D., Messner, A., Martins, P. T., Delogu, F., Alamri, S., & Boeckx, C. (2017) · PLOS ONE · doi:10.1371/journal.pone.0185306 · Cited by 174 · see citing works
Scleral appearance is not a correlate of domestication in mammals
Caspar, K. R., Hüttner, L., & Begall, S. (2023) · Zoological Letters · doi:10.1186/s40851-023-00210-z · Cited by 8 · see citing works
- Authors
- Singh, N., Albert, F. W., Plyusnina, I., Trut, L., Pӓӓbo, S., & Harvati, K.
- Affiliations
- Pennsylvania State University (US)
- University of Minnesota (US)
- Institute of Cytology and Genetics (RU)
- Senckenberg Centre for Human Evolution and Palaeoenvironment (DE)
- Corresponding author
- Singh, Nandini
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-04-03
- Volume
- 12
- Issue
- 4
- Pages
- e0175043
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5378367
- OpenAlex
- W2605254503
- Cited by
- 42
- References
- 53
- Citations by year
- 2025: 4 · 2024: 6 · 2023: 2 · 2022: 8 · 2021: 4 · 2020: 3 · 2019: 6 · 2018: 8 · 2017: 1
- FWCI
- 6.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (INST 37/706)
- Max-Planck-Gesellschaft
- Topics
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- domestication syndrome, neural crest cells, facial morphology, craniofacial morphology, tameness, defensive aggression, silver fox, rats, sexual dimorphism, skull shape, geometric morphometrics, animal domestication
- MeSH terms
- Domestication, Aggression, Animals, Animals, Domestic, Behavior, Animal, Breeding, Face, Facial Expression, Foxes, Skull, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review