Anastasia V. Kharlamova

Sign and strength of emotional arousal: vocal correlates of positive and negative attitudes to humans in silver foxes ( Vulpes vulpes )

Summary The hypothesis of similarity in trends of acoustic characteristics regardless of the sign of emotional arousal, positive or negative, has been advanced based on human vocalizations. For non-human mammals, testing is complicated because the same stimulus cannot evoke opposite (positive and negative) internal states, to trigger the respective vocalizations. To resolve this concern, we designed an experimental procedure using Tame and Aggressive strains of silver foxes, with genetically predetermined positive or negative emotional responses to humans respectively. We analyzed features of vocalizations produced by callers at different fox‐human distances, assuming changes in vocal responses reflect the shifts of human-related positive arousal in Tame foxes and human-related negative arousal in Aggressive foxes. Both strains showed similar trends for changes in calling rate and proportion of time spent vocalizing toward higher levels in response to greater emotional arousal, positive in Tame foxes and negative in Aggressive foxes. At the same time, strains showed distinctive trends for the proportions of different call types and maximum amplitude frequency. We infer that the variables with similar trends reflect the strength of emotional arousal, regardless of triggering internal states, whereas variables with distinctive trends are specifically related to the sign of emotion in silver fox.

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 x Aggressive), A-Backcrosses (Aggressive x Hybrid) and T-Backcrosses (Tame x 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.

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.

26 The Genetics of Domesticated Behavior in Canids: What Can Dogs and Silver Foxes Tell Us about Each Other?

Domesticated animals display distinct differences in behavior, morphology, and physiology from their wild counterparts. They usually exhibit reduced aggressiveness, increased social tolerance among conspecifics, and reduced sensitivity to environmental changes (for review, see Sachser 1998; Price 2002). The complex suite of modified social behaviors and cognitive abilities that results from domestication specifically includes tameness, the ability to interact with humans in a positive way. An understanding of the genetics of tameness in canids should provide new insight into the mechanisms underlying social behavior in canids and other species, and into the broader phenomenon of domestication as a whole. Herein, we discuss strategies for identification of the genetic roots of tame behavior in canids. For the purposes of this chapter, we refer to this friendly, dog-like behavior as tameness. The mutual ability of dogs and humans to communicate, and to interact socially with each other, is so commonplace that it is often not recognized for how strange a phenomenon it represents. The sentiment “She is almost human—just cannot speak” would be immediately understood by anyone familiar with the relationship between dogs and their human companions. Without a word from them, we understand our dogs very well. We can read their body language, facial expressions, habits, and emotional states; and they can read ours. They can understand our mood, intent, tone of voice, and words from our language. Sometimes it is hard to credit that the modern dog ( Canis familiaris ) is such a recent and close relative of the gray wolf...

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.

Vocalization toward conspecifics in silver foxes (Vulpes vulpes) selected for tame or aggressive behavior toward humans

We examined the production of different vocalizations in three strains of silver fox (unselected, aggressive, and tame) attending three kinds of behavior (aggressive, affiliative, and neutral) in response to their same-strain conspecifics. This is a follow-up to previous experiments which demonstrated that in the presence of humans, tame foxes produced cackles and pants but never coughed or snorted, whilst aggressive foxes produced coughs and snorts but never cackled or panted. Thus, cackle/pant and cough/snort were indicative of the tame and aggressive fox strains respectively toward humans. Wild-type unselected foxes produced cough and snort toward humans similarly to aggressive foxes. Here, we found that vocal responses to conspecifics were similar in tame, aggressive and unselected fox strains. Both cackle/pant and cough/snort occurred in foxes of all strains. The difference in the use of cackle/pant and cough/snort among these strains toward humans and toward conspecifics suggest that silver foxes do not perceive humans as their conspecifics. We speculate that these vocalizations are produced in response to a triggering internal state, affiliative or aggressive, that is suppressed by default in these fox strains toward humans as a result of their strict selection for tame or aggressive behavior, whilst still remaining flexible toward conspecifics.

Genetic regulation of canine skeletal traits: trade-offs between the hind limbs and forelimbs in the fox and dog

Genetic variation in functionally integrated skeletal traits can be maintained over 10 million years despite bottlenecks and stringent selection. Here, we describe an analysis of the genetic architecture of the canid axial skeleton using populations of the Portuguese Water Dog Canis familiaris) and silver fox (Vulpes vulpes). Twenty-one skeletal metrics taken from radiographs of the forelimbs and hind limbs of the fox and dog were used to construct separate anatomical principal component (PC) matrices of the two species. In both species, 15 of the 21 PCs exhibited significant heritability, ranging from 25% to 70%. The second PC, in both species, represents a trade-off in which limb-bone width is inversely correlated with limb-bone length. PC2 accounts for approximately 15% of the observed skeletal variation, approximately 30% of the variation in shape. Many of the other significant PCs affect very small amounts of variation (e.g., 0.2-2%) along trade-off axes that partition function between the forelimbs and hind limbs. These PCs represent shape axes in which an increase in size of an element of the forelimb is associated with a decrease in size of an element of the hind limb and vice versa. In most cases, these trade-offs are heritable in both species and genetic loci have been identified in the Portuguese Water Dog for many of these. These PCs, present in both the dog and the fox, include ones that affect lengths of the forelimb versus the hind limb, length of the forefoot versus that of the hind foot, muscle moment (i.e., lever) arms of the forelimb versus hind limb, and cortical thickness of the bones of the forelimb versus hind limb. These inverse relationships suggest that genetic regulation of the axial skeleton results, in part, from the action of genes that influence suites of functionally integrated traits. Their presence in both dogs and foxes suggests that the genes controlling the regulation of these PCs of the forelimb versus hind limb may be found in other tetrapod taxa.

Directional Asymmetry in the Limbs, Skull and Pelvis of the Silver Fox (V. vulpes)

Directional asymmetry (DA) is a characteristic of most vertebrates, most strikingly exhibited by the placement of various organs (heart, lungs, liver, etc.) but also noted in small differences in the metrics of skeletal structures such as the pelvis of certain fish or sauropsids. We have analyzed DA in the skeleton of the fox (V. vulpes), using ∼1,000 radiographs of foxes from populations used in the genetic analysis of behavior and morphology. Careful measurements from this robust data base demonstrate that: 1) DA occurs in the limb bones, the ileum, and ischium and in the mandible; 2) regardless of the direction of the length asymmetry vector of a particular skeletal unit, the vectorial direction of length is always opposite to that of width; 3) with the exception of the humerus and radius, there is no correlation or inverse correlation between vectorial amplitudes or magnitudes of bone asymmetries. 4) Postnatal measurements on foxes demonstrate that the asymmetry increases after birth and continues to change (increasing or decreasing) during postnatal growth. 5) A behavior test for preferential use of a specific forelimb exhibited fluctuating asymmetry but not DA. None of the skeletal asymmetries were significantly correlated with a preferential use of a specific forelimb. We suggest that for the majority of fox skeletal parameters, growth on the right and left side of the fox are differentially biased resulting in fixed differences between the two sides in either the rate of growth or the length of the period during which growth occurs. Random effects around these fixed differences perturb the magnitude of the effects such that the magnitudes of length and width asymmetries are not inversely correlated at the level of individual animals. J. Morphol., 2010.

Effects of selection for behavior, human approach mode and sex on vocalization in silver fox

This study presents a first direct comparison of vocal type, call rate and time spent vocalizing among Unselected, Tame and Aggressive strains of silver fox (Vulpes vulpes) in three modes of human approach (Provoking, Approach–Retreat, and Static). Also, it provides a first comparison of male and female vocal output in the Provoking test. Vocal types were found strain-specific irrespective of the fox sex or the test. Males had higher call rates and spent shorter times vocalizing than females. These results support the evidence of genetic-based emotional states, triggering vocal behavior in silver fox strains, and suggest sex dimorphism in vocal activity toward humans.

6 Morphology and Behavior: Are They Coupled at the Genome Level?

In all organisms, behavior and morphology are inextricably coupled. Morphology constrains the range of behavioral patterns, and behavior regulates and modifies morphological function. Over centuries, this constraint has been recognized in the selective breeding of dogs to perform specific tasks. Here, we explore the genetic coupling of morphology and behavior in a fox model system: the heritable morphological variation that has accompanied selection for tame and aggressive behavioral traits in the silver fox. In what follows, we demonstrate that similar functional trade-offs in morphology are found in both foxes and dogs and that this morphological variation may be concomitant with behavioral variation. Finally, we describe preliminary results from experiments designed to test whether these two phenotypes are related at the genetic level (thus co-selected) or have become associated serendipitously as a result of random genetic drift and founder effects. The red fox, Vulpes vulpes , of which the silver fox is a subspecies, is the out-group for modern canids. Its phylogenetic lineage has been separated from Canis familiaris for about 10 million years (Wayne 1993). V. vulpes has the largest natural geographic distribution of any terrestrial mammal other than humans. It occupies habitats ranging from mixed forest to alpine tundra, from sand dunes to urban outskirts (Nowak and Paradiso 1991; Sheldon 1992). Associated with this diversity of habitats is a wide range of anatomical configurations and a behavioral plasticity that makes the red fox the bane of chicken farmers, the favorite of hunting sportsmen, and a mythic symbol of crafty intelligence...