Research Article: Facial shape differences between rats selected for tame and aggressive behaviors

Date Published: April 3, 2017

Publisher: Public Library of Science

Author(s): Nandini Singh, Frank W. Albert, Irina Plyusnina, Lyudmila Trut, Svante Pӓӓbo, Katerina Harvati, Sergio Pellis.


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.

Partial Text

The classic selection experiments by Dmitry Belyaev have demonstrated that breeding animals for tameness can lead to a suite of physiological, cognitive and morphological changes similar to those associated with domestication [1,2]. Key morphological traits that comprise the domestication syndrome include changes in adreno-cortical responses, coat coloration, brain size, body size and craniofacial size and shape [3–5]. According to Belyaev, behavior–specifically tameness–was the driving factor behind all the traits present in domesticated animals [2]. Selective breeding of animals allows for a closer look at the initial factors that led to domestication. Behavior is regulated by neurotransmitters and hormones, which when altered by strict selection for a particular trait, can cause changes in key developmental processes, thereby potentially affecting the phenotype [6].

The animals we studied here are the same animals described in the original characterization of the Leipzig populations of these rats [4]. Briefly, the rats that had been brought to Leipzig were from the 64th generation of selection. The selection regime in Novosibirsk entailed testing the reaction of these rats to humans, measured through the rats’ reaction to an approaching hand. The animals studied here are from the 2nd and 3rd generation born in Leipzig. All animals were maintained in identical cages and conditions, and treated exactly the same way, including the level of interaction with the human handlers. Animals were weighed, anaesthetized with CO2 and killed by cervical dislocation. Further details on the experimental regime and maintenance of the rat colonies can be obtained in Albert et al. [4]. All procedures were reviewed and approved by the regional government of Saxony (TVV 29/05), Germany.

Animal and plant domestication has been a focus of intense research at least since the time of Darwin [51]. Experimental animal models have added a new dimension to archaeological evidence by providing novel ways in which we can address a number of questions regarding the genetic and developmental origins of animal domestication. Our findings show that targeted selection for reduced aggression in Belyaev’s rats is accompanied by changes in the face, which is entirely derived from NCC, and that those changes are independent of cranial size. This result suggests that the craniofacial changes in the tame rats might be a developmental-genetic ‘side effect’ of selection for tameness. However, the tame rats do not perfectly mimic domesticated animals in that they do not show a notable reduction in facial sexual dimorphism.




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