Hecht Erin E, Kukekova Anna V, Gutman David A, Acland Gregory M, Preuss Todd M, Trut Lyudmila N
Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138
Department of Animal Sciences, College of Agriculture, Consumer, and Environmental Sciences, University of IL Urbana-Champaign, Urbana, IL 61801.
J Neurosci. 2021 Jul 14;41(28):6144-6156. doi: 10.1523/JNEUROSCI.3114-20.2021.
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. 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.
俄罗斯农场狐狸实验是一项持续时间异常长且控制良好的研究,旨在重现狼到狗的驯化过程。因此,它为研究行为进化的神经机制提供了一个前所未有的窗口。在此,我们报告了在30只雄性狐狸大脑样本中,因选择温顺或对人类的攻击性反应而导致的灰质形态的进化变化。与关于驯化对大脑大小影响的现有观点相反,温顺的狐狸并没有表现出脑容量减少。相反,与未经行为方面刻意选择培育的传统农场狐狸相比,温顺和攻击性品系的灰质体积都增加了。此外,温顺和攻击性增大的区域有很大重叠,包括运动、体感和前额叶皮层、杏仁核、海马体和小脑的部分区域。我们还观察到分布在不同灰质网络中的形态协变差异。在一个前额叶 - 小脑网络中,这种协变沿着温顺 - 攻击性行为轴区分了这三个群体。令人惊讶的是,一个前额叶 - 下丘脑网络将温顺和攻击性狐狸与传统品系区分开来。这些发现表明,对相反行为的选择可以以相似的方式影响大脑形态。驯化是地球上生命最大且最迅速的进化转变之一。然而,其神经关联在很大程度上尚不清楚。在此,我们报告了在具有开创性的俄罗斯农场狐狸实验中,针对温顺或攻击性进行选择性育种的神经解剖学后果。与一群传统农场养殖的对照狐狸相比,温顺的狐狸在额叶前皮质和下丘脑显示出神经解剖学变化,这与狼到狗的转变相似。然而,令人惊讶的是,攻击性狐狸也表现出类似的变化。此外,相对于对照,两个品系的灰质体积都增加了。这些结果表明,对相反行为的选择可导致类似的大脑适应性变化,现有的关于驯化中大脑变化的观点可能需要修正,并且显著的神经解剖学变化可以在不到100代的时间跨度内迅速进化。