Neuromorphological Changes following Selection for Tameness and Aggression in the Russian Farm-Fox experiment

Erin E Hecht; Anna V Kukekova; David A Gutman; Gregory M Acland; Todd M Preuss; Lyudmila N Trut

doi:10.1523/JNEUROSCI.3114-20.2021

Neuromorphological Changes following Selection for Tameness and Aggression in the Russian Farm-Fox experiment

J Neurosci. 2021 Jul 14;41(28):6144-6156. doi: 10.1523/JNEUROSCI.3114-20.2021.

Authors

Erin E Hecht¹, Anna V Kukekova², David A Gutman³, Gregory M Acland⁴, Todd M Preuss⁵, Lyudmila N Trut⁶

Affiliations

¹ Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138 erin_hecht@fas.harvard.edu.
² Department of Animal Sciences, College of Agriculture, Consumer, and Environmental Sciences, University of IL Urbana-Champaign, Urbana, IL 61801.
³ School of Medicine, Emory University, Atlanta, GA 30322.
⁴ Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, New York, 14853.
⁵ Yerkes National Primate Research Center, Emory University, Atlanta, GA 30322.
⁶ Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia, 630090.

Abstract

The Russian farm-fox experiment is an unusually long-running and well-controlled study designed to replicate wolf-to-dog domestication. As such, it offers an unprecedented window onto the neural mechanisms governing the evolution of behavior. Here we report evolved changes to gray matter morphology resulting from selection for tameness versus aggressive responses toward humans in a sample of 30 male fox brains. Contrasting with standing ideas on the effects of domestication on brain size, tame foxes did not show reduced brain volume. Rather, gray matter volume in both the tame and aggressive strains was increased relative to conventional farm foxes bred without deliberate selection on behavior. Furthermore, tame- and aggressive-enlarged regions overlapped substantially, including portions of motor, somatosensory, and prefrontal cortex, amygdala, hippocampus, and cerebellum. We also observed differential morphologic covariation across distributed gray matter networks. In one prefrontal-cerebellum network, this covariation differentiated the three populations along the tame-aggressive behavioral axis. Surprisingly, a prefrontal-hypothalamic network differentiated the tame and aggressive foxes together from the conventional strain. These findings indicate that selection for opposite behaviors can influence brain morphology in a similar way.SIGNIFICANCE STATEMENT Domestication represents one of the largest and most rapid evolutionary shifts of life on earth. However, its neural correlates are largely unknown. Here we report the neuroanatomical consequences of selective breeding for tameness or aggression in the seminal Russian farm-fox experiment. Compared with a population of conventional farm-bred control foxes, tame foxes show neuroanatomical changes in the PFC and hypothalamus, paralleling wolf-to-dog shifts. Surprisingly, though, aggressive foxes also show similar changes. Moreover, both strains show increased gray matter volume relative to controls. These results indicate that similar brain adaptations can result from selection for opposite behavior, that existing ideas of brain changes in domestication may need revision, and that significant neuroanatomical change can evolve very quickly, within the span of <100 generations.

Keywords: aggression; canids; domestication; farm-fox experiment; neuroimaging; social behavior.

Grants and funding

R01 GM120782/GM/NIGMS NIH HHS/United States