Animal evolution during domestication: the domesticated fox as a model

Abstract

We review the evolution of domestic animals, emphasizing the effect of the earliest steps of domestication on its course. Using the first domesticated species, the dog (Canis familiaris), for illustration, we describe the evolutionary peculiarities during the historical domestication, such as the high level and wide range of diversity. We suggest that the process of earliest domestication via unconscious and later conscious selection of human-defined behavioral traits may accelerate phenotypic variations. The review is based on the results of a long-term experiment designed to reproduce early mammalian domestication in the silver fox (Vulpes vulpes) selected for tameability or amenability to domestication. We describe changes in behavior, morphology and physiology that appeared in the fox during its selection for tameability, which were similar to those observed in the domestic dog. Based on the data of the fox experiment and survey of relevant data, we discuss the developmental, genetic and possible molecular genetic mechanisms underlying these changes. We ascribe the causative role in evolutionary transformation of domestic animals to the selection for behavior and to the neurospecific regulatory genes it affects.

Fig. 1

Variability range in dogs for: A: body size (Chinese crested, pekingese and bullmastiff); B: body shape (greyhound and English bulldog); C: coat types (hairless terrier and komondor).

Fig. 2

Representatives of different families and orders show the most specific morphological markers of domestication, white spotting on the head (top row) and floppy ears (bottom row): A: Horse (Equus caballus): Order Perissodactyla, Equidae family, breed, the Soviet heavy draught-horse; B: Cow (Bos taurus): Order Artiodactyla, Bovidae family, Aberdin-Angus breed (top), banteng breed (bottom); C: Pig (Sus scrofa domestica): Order Artiodactyla, Suidae family, hybrid of the Vietnamese breed (top), Landrace breed (bottom); D: Sheep (Ovis): Order Artiodactyla, Bovidae family, Romanov breed (top), balbas breed (bottom); E: Dog (Canis familiaris): Order Carnivora, The Canidae family, a Boston terrier (top), a pug (bottom); F: Rabbit (Oryctolagus cunticulus): Order Lagomorpha, Leporidae family, a Holland white-black (top), a German ram (bottom).

Fig. 3

Behavior of foxes of the farm-bred populations (top row) and of the population selected for tameability (bottom row): A: A fox showing the aggressive response to humans; B: A fox showing the avoidance response to humans; C: A fox weakly expressing the wild-type aggressive-avoidance response to humans; D-F: Domesticated foxes referred to the behavioral elite. F: from left to right: Prof. K.G. Lark (University of Utah, Salt Lake City), Prof. L.N. Trut (Institute of Cytology and Genetics, Novosibirsk), Prof. G.M. Acland (Cornell University, Ithaca) with domestic foxes.

Fig. 4

A schematic representation of the results of the fox domestication experiment. A: Transformation of fox behavior resulting from selection for tameability.

1. Left: a fox of the farm-bred population unselected for behavior. Foxes of this population show the typical aggressive response to human.

2. Right: a fox of the experimental domesticated population. The dog-like behavior of foxes of this population is the result of many years of selection for tameability.

B – E: Activity of the HPA axis in farm-bred and domesticated foxes. Farm-bred foxes are shown in grey, the domesticated are in red. B: Hypothalamic CRF (CRFmRNA/18SmRNA) and pituitary POMC (POMCmRNA/18SmRNA) gene expression, ACTH (pg/ml) and cortisol (μg/dl) level in farm-bred and domesticated foxes. C: Age-related changes in plasma cortisol level in farm-bred and domesticated foxes: 1) farm-bred foxes with aggressive response to human, 2, 3) foxes of the domesticated population with low (2), and high (3) domestication scores. D: Total time of locomotion, an indicator of exploratory behavior, and plasma cortisol level in farm-bred and domesticated foxes at the age of 1-2 months: locomotion is plotted on the graph; plasma cortisol level is represented as bars. E: Plasma cortisol in silver foxes during pregnancy and lactation. F – J: Dog-like morphological changes arisen in foxes of the domesticated population: F: Similarity of coat depigmentation between dogs and foxes: Left, a border collie; Right, a tame fox. G: Tail carriage, curly tail: Left, an Islandsk Farehund; Right, a tame fox. H: Ears are floppy and face skull is widened in some pups of tame foxes: Left, a pug; Right, a tame fox pup. I: Long jaw (elongation of the lower jaw) in the English bulldog occurs among tame foxes: Left, an English bulldog; Right, a tame fox. J: Elongation of face skull in certain dog breeds and tame foxes: Left, a Pharaoh hound, Right, a tame fox.

Fig. 5

Specific markers of domestication. A: Two different phenotypic changes in a Ss heterozygote : the Star depigmentation and a floppy right ear. B: Homozygote for the Star mutation (SS). C: Phenotypic similarity between brown mottling in fox and dog.