Photoperiodic control of gonadal endocrine function in silver-gray foxes and its alteration during domestication

Studies have been made on the level of estradiol and progesterone in domesticated and nondomesticated female silver foxes under different photoperiodic regime. The duration of the "light--darkness" cycle was equal to 24 h. Total duration of the light period was equal to 9 1/2 h; illumination was natural for 7 h, being artificial for the rest 2 1/2 h in a dark part of a day. It was demonstrated that additional illumination affects the hormonal level and sexual activity, the effect being dependent on the particular time of illumination. Nocturnal illumination significantly increased the level of sex hormones in the blood, domesticated animals being more sensitive as compared to nondomesticated ones.     

The effect of the domestication of Norway rats and silver foxes on the serotonin S1A- and S2-receptors of the brain]

The specific radioligand binding of serotonin 5-HT1A and 5-HT2 receptors was determined in the frontal cortex and in the hypothalamus of Norway rats and silver foxes. Aggressive wild rats and silver foxes and animals selected for many generations for nonaggressive behavior towards man (domestication) were compared. The binding of the 5-HT1A receptors was found to be significantly higher in domesticated Norway rats and lower in domesticated foxes than in aggressive animals. The specific binding of the 5-HT2 receptors was found to be similar in aggressive and domesticated animals, both in rats and foxes. The data obtained indicate the involvement of 5-HT1A receptors in the hypothalamus into the process of domestication.     

Methodological approach to genetic-selection analysis of social behavior of animals (Using as an example domestic behavior of the silver fox

Social behaviour of animals, i.e. interspecies contacts, were studied in a population of silver foxes in the longitudinal model domestication experiment. Three social behaviour traits were analysed: contactibility, critical distance and domestication index. The latter trait is a linear function of elementary behaviour reactions, postures induced by man which is determined by the principal components method. The most valiable selection phenotype for further modelling of domestication, as shown by the capacity to adequately reflect a pattern of genotype--environment interaction, the structure of correlation ratios for different forms of behaviour and the level of genetic relationships between relatives, is the domestication index.     

Adrenal function in different phases of the estrous cycle in the domesticated silver fox, Vulpes fulvus

Experiments were made on silver foxes from a population which had been selected for 10 to 15 generations for the domestic behaviour and on animals from a control, unselected population. In females from both populations, studies were made of the level of 11-OHCS in the blood serum, in vitro production of 11-OHCS, the size of fascicular zone in the adrenal cortex, the volume of cellular nuclei and nucleoli, as well as the reaction of the adrenals in vitro to 2 doses of ACTH (1 and 5 units/g of the adrenals) during anestrus, proestrus and estrus. In control females, all the characters investigated significantly increased from anestrus to proestrus. In domesticated females, no changes in the production of 11-OHCS in vitro or changes in morphological features of the fascicular zone were observed in the course of estrous cycle. During proestrus, the adrenals of the domesticated animals were not able to increase the production of 11-OHCS in vitro after application of ACTH. The decrease in the reactivity of the adrenals to the effect of ACTH is presumably the main cause why in unselected females the adrenal are not activated during proestrus. Therefore, in the course of selection for the domestication type of behaviour, species specific dynamics of activation of the adrenals during estrous cycle is lost.     

Genetics and phenogenetics of the hormonal characteristics of animals. VII. Correlation between brain serotonin and the hypothalamo-pituitary-adrenal system in domesticated and undomesticated silver foxes during emotional stress

Two groups of silver foxes, selected according their behaviour with respect to man and non-selected ones, were exposed to restriction-induced stress. It was found that changes in the level of brain serotonin and its main metabolite, 5-hydroxyindolacetic acid, and elevation of plasma corticosteroids concentration in domesticated (tame) silver foxes were much less pronounced than in non-domesticated (non-tame) animals. Positive relationship between type of behaviour, brain serotonin metabolism and pituitary-adrenal axis response to stress was observed. It is suggested that such correlative pattern as changed pituitary-adrenal axis responses in domesticated animals may be due to changes in metabolism of controlling this axis brain transmitter serotonin.     

Explosive vocal activity for attracting human attention is related to domestication in silver fox

Domestication affects behavioral and vocal responses, involved in communication with humans; in particular, those that attract human attention. In this study, we found that silver foxes of Tame strain, experimentally domesticated for a few tenses of generation, displayed bursts of vocal activity during the first minute after appearance of an unfamiliar human, that faded quickly during the remaining time of the test, when the experimenter stayed passively before the cage. Distinctively, foxes of Aggressive strain, artificially selected for tenses of generation for aggressive behavior toward humans, and the control group of Unselected for behavior silver foxes kept steady levels of vocal activity for the duration of the tests. We found also that Aggressive foxes vocalized for a larger proportion of time than Unselected foxes for all 5 min of the test. We discuss the obtained data in relation to proposal effects of domestication on mechanisms directed to involving people into human-animal interactions and structural similarity between human laughter and vocalization of Tame foxes.     

Brain tyrosine hydroxylase activity in behavior-selected silver foxes

In two groups of silver foxes--i.e. selected by the domestic type of behaviour and aggressive ones--studies have been made on the activity of the key enzyme in biosynthesis of catecholamines--i.e. tyrosine hydroxylase from the brain. Domesticated animals exhibited higher enzymic activity in the locus coeruleus, hypothalamus and cortex. Animals from both groups did not differ with respect to the level of tyrosine hydroxylase activity in the corpus striatum. The enzymic reactions of homogenates from locus coeruleus region of the brain in both groups of animals, as well as homogenates from the corpus striatum of the brain of aggressive animals exhibited low and approximately equal values of Michaelis constant for tyrosine. The value of KM was 3 times higher in the hypothalamus in both groups of foxes and in the corpus striatum of tame animals. Presumably, selection of silver foxes for the domestic type of behaviour resulted in the increase of biosynthesis of catecholamines in the brain due to the increase in the number of enzyme molecules. The increase in the activity of tyrosine hydroxylase in noradrenaline system of the brain may be associated with changes in the behavioural pattern of animals resulting from selection.     

Interhemisphere neurochemical differences in the brain of silver foxes selected for behavior and the problem of directed asymmetry

The study deals with the mechanisms that bring about a directional asymmetry in the expression of some morphological traits observed in some animals subjected to experimental domestication. The key role in the integration of development is attributed to the genetic systems controlling the activity of brain neurotransmitter systems. Therefore, the investigation of directional asymmetry of morphological traits began with the analysis of interhemispheral differences in neurotransmitter activity in animal lines selected for domestic and aggressive behavior. Experiments on silver foxes reveal interhemispheral differences in the dopaminergic system emerging in the striatum. An increased dopamine level is observed in the right half of the striatum of aggressive foxes and in both right and left halves of the striata of domestic foxes. On the basis of the literature data, it is suggested that the considerable increase in the dopamine level in the right halves of the striata of both aggressive and domestic animals is related to a genetic increase in the manifestation of emotional response in both lines, whereas its increase in the left half of the striatum of domesticated foxes may be related to a correlated deterioration of the function of the pituitary-adrenal system.     

Genetics and phenogenetics of the hormonal characteristics of animals. II. Changes in the reactivity of the pituitary-adrenal system and influence of the sex glands in selection of silver-black foxes by behavior]

Seasonal changes in the reactivity of adrenal cortex to ACTH and of the pituitary-adrenal system to psychic stress in intact and castrated domesticated (tame) and non-domesticated (non-tame) silver foxes of both sexes were studied. It is demonstrated that in tame foxes there are differences among the intact and castrated animal in their reaction to ACTH and psychic stress. These differences are maifested especially in autumn (September, October) which is the period of extra-seasonal sexual activity for domesticated animals. This points to the fact that the sex glands exert a great influence on the condition of central regulating mechanisms of the pituitary-adrenal complex and that the selection of silver foxes for tame behaviour changes the functional state of these mechanisms through the change of the functional state of the sex glands.     

Genetics and phenogenetics of hormonal characteristics of animals. VIII. Analysis of the variability of the corticosteroid function of the adrenal cortex of silver foxes during their domestication

The contribution of genetic and environmental components in phenotype variety of corticosteroid adrenal function was studied in undomesticated and domesticated silver foxes during postnatal ontogenesis. The variation of basal and stress plasma corticosteroid level in animals aged 2, 4, 6, 8 months and in vitro secretion of the adrenal gland at the age 8 months was analysed. Significant genotype-depended variability was only demonstrated in undomesticated foxes under stress stimulation conditions. This phenomenon is manifested from the fourth month of life. However, significant genotype-depended variability was already revealed under basal conditions in domesticated foxes, on initial steps of postnatal ontogenesis. The peculiarities of genetic variability of adrenocortical function in foxes selected for domestication are discussed.     

Kind granddaughters of angry grandmothers: The effect of domestication on vocalization in cross-bred silver foxes

The genetic basis of the effects of domestication has previously been examined in relation to morphological, physiological and behavioural traits, but not for vocalizations. According to Belyaev [Belyaev, D.K., 1979. Destabilizing selection as a factor in domestication. J. Hered. 70, 301-308], directional selection for tame behaviour toward humans resulted in domestication. This hypothesis has been confirmed experimentally on the farm-bred silver fox Vulpes vulpes population that has undergone 45 years of artificial selection for tameness and 35 years of selection for aggressiveness. These foxes, with their precisely known attitudes toward people, provide a means of examining vocal indicators of tameness and aggressiveness to establish the genetic basis for vocal production in canids. We examined vocalizations toward people in foxes selected for tameness and aggressiveness compared to those of three kinds of crosses: Hybrids (Tame × Aggressive), A-Backcrosses (Aggressive × Hybrid) and T-Backcrosses (Tame × Hybrid). We report the effects of selection for tameness on usage and structure of different vocalizations and suggest that vocal indicators for tameness and aggressiveness toward people are discrete phenotypic traits in silver foxes.     

Serotonin receptors in the brain of animals selected for their domesticated type of behavior

Participation was studied of central serotonin receptors of the first and second types in behaviour change of animals selected by the character of defensive reaction to man. Serotonin receptors were determined by radioligand method by binding of the brain preparations 3H-serotonin and 3H-spiperone. An increase of C2 receptors number was found in the frontal brain cortex of the tame brown rats in comparison with the aggressive ones. Differences were not found in specific C1-receptor binding in the frontal brain cortex of tame and aggressive brown rats, silver foxes and American minks in various relatively early selection stages. It is supposed that disappearance of aggressive reaction to man at domestication is connected with an increase of C2 receptors number.     

Change in tryptophan hydroxylase activity in the brain of silver foxes and wild Norway rats in the course of selection according to behavior

The activity of tryptophan hydroxylase, the key enzyme of serotonin biosynthesis, was determined in the brain of silver foxes and wild rats selected, according to domestic or aggressive behavior, in respect to man. Significant increase of enzyme activity in midbrain of both domesticated rats and domesticated foxes was found, in comparison with that of aggressive animals. It was suggested that genetic mechanisms of the selection according to aggressive behavior, involve the changes of genes responsible for the synthesis of serotonin, the brain neurotransmitter which inhibits this type of behavior.     

Testosterone production by the fetal testes of silver foxes selected for their domesticated behavior]

Testosterone content was determined by radioimmune assay in the testes of silver foxes between the 31st and 50th days of gestation. Small quantities of testosterone were found in the testes already at the 31st day of prenatal life, gradually increasing up to a maximum value at the 50th day. No significant difference in testosterone content was found between domesticated and undomesticated silver foxes during prenatal life. It is suggested that selection for domesticated behaviour affects rather central control of endocrine functions than steroid biosynthesis in the testes.     

Inter- and intraspecific competition between the fox species Alopex lagopus and Vulpes vulpes: an evaluation trial under penned conditions

This study compared competition capacity and dominance relations between arctic foxes (Alopex lagopus) and red foxes (Vulpes vulpes). Experiments were carried out in semi-natural earthen floor enclosures using farm-bred colour types of both species (blue fox and silver fox) as subjects. Results of the dominance scoring and open field behaviour after weaning in August-September showed that blue foxes dominated over silver foxes. Thereafter, the situation gradually became reversed and silver foxes were dominant during the breeding and whelping seasons. Housing both species together from weaning produced more curious animals as compared to when these species were placed in common quarters after the autumn equinox. In the case of blue foxes, the male dominated highly over all females. In silver foxes, the difference in dominance between the sexes was, however, less pronounced. The most dominant individuals in the study groups were typically among the heaviest. Breedings and whelpings succeeded better in silver than in blue foxes. However, none of litters born survived more than one week. The present results support the conclusion that when both fox species are housed together, Vulpus vulpus tends to dominate over Alopex lagopus. Received: 22 March 1996/Accepted: 30 June 1996     

The gradual vocal responses to human-provoked discomfort in farmed silver foxes

Vocal indicators of welfare have proven their use for many farmed and zoo animals and may be applied to farmed silver foxes as these animals display high vocal activity toward humans. Farmed silver foxes were selected mainly for fur, size, and litter sizes, but not for attitudes to people, so they are fearful of humans and have short-term welfare problems in their proximity. With a human approach test, we designed here the steady increase and decrease of fox–human distance and registered vocal responses of 25 farmed silver foxes. We analyzed the features of vocalizations produced by the foxes at different fox–human distances, assuming that changes in vocal responses reflect the degrees of human-related discomfort. For revealing the discomfort-related vocal traits in farmed silver foxes, we proposed and tested the algorithm of “joint calls,” equally applicable for analysis of all calls independently on their structure, either tonal or noisy. We discuss that the increase in proportion of time spent vocalizing and the shift of call energy toward higher frequencies may be integral vocal characteristics of short-term welfare problems in farmed silver foxes and probably in other captive mammals.     

Phenogenetic analysis of various changes in the color of fur in silver foxes originated during domestication

Quantitative and qualitative analysis of pigmentation in "singne"-type fur color mutation arising in silver foxes during domestication, was made. It was shown that the decrease in quantity of eumelanine in hair and uneven distribution of pigment granules lengthwise the hair were the reason for formation of "singnes".     

Role of the amygdala in the behavior of domesticated and aggressive foxes

Influence was studied of the bilateral electric coagulation of the basolateral part of the amygdala on the behaviour in unknown environment and on the attitude to the man of domesticated and aggressive foxes. Increase of exploratory behaviour with enhancing of motor activity was observed in all foxes after amygdala ablation. At the same time a decrease of positive emotional reactions to man was observed in the domesticated animals, while in the aggressive foxes defensive reactions to man and in unknown environment were weakened.     

The brain catecholamines during domestication of the silver fox Vulpes fulvus

Studies have been made on the content of catecholamines (noradrenaline and dopamine) as well as metabolites of dopamine (3,4-dihydroxyphenylacetic and homovanillic acids) in the brain structures of silver foxes which differ in their handling reactions. The level of noradrenaline was found to be significantly higher in the anterior hypothalamus of domesticated animals; no differences in noradrenaline content were found in the frontal cortex, hippocamp, posterior hypothalamus and midbrain in animals from aggressive and domesticated groups. Dopamine content was higher in the tuberculum olfactorium of domesticated animals, being lower in the striatum and n. accumbens. Metabolite level remained unaffected which is presumably due to changes in dopamine synthesis in the investigated structures. It was concluded that domestication of animals favours the specimens with an altered state of catecholaminergic system of the brain.     

Component analysis of craniologic characters of silver foxes (Vulpes fulvus Desm.) and their changes arising under domestication]

The data on cranial measurements performed in silver foxes indicate that there are differences in sizes measured between the farm foxes--bred population and the population selected for domestication. A method of principal components was used to analyse the cranial measurements and their changes under domestication. The first component covers about 50% of cranial diversity, which is interpreted as variation in the total skull size. This component clearly separates the two sexes, but not different populations. The second component presumably reflects the growth rate allometry between the skull length and width. The third and fourth components are measurements of skull width; the fifth one reflects the sizes of brain skull. None of these components clearly separate the foxes from farm--bred and domesticated populations. However, some differences in distribution are observed.