Genomic responses to selection for tame/aggressive behaviors in the silver fox (Vulpes vulpes).

Animal domestication efforts have led to a shared spectrum of striking behavioral and morphological changes. To recapitulate this process, silver foxes have been selectively bred for tame and aggressive behaviors for more than 50 generations at the Institute for Cytology and Genetics in Novosibirsk, Russia. To understand the genetic basis and molecular mechanisms underlying the phenotypic changes, we profiled gene expression levels and coding SNP allele frequencies in two brain tissue specimens from 12 aggressive foxes and 12 tame foxes. Expression analysis revealed 146 genes in the prefrontal cortex and 33 genes in the basal forebrain that were differentially expressed, with a 5% false discovery rate (FDR). These candidates include genes in key pathways known to be critical to neurologic processing, including the serotonin and glutamate receptor pathways. In addition, 295 of the 31,000 exonic SNPs show significant allele frequency differences between the tame and aggressive populations (1% FDR), including genes with a role in neural crest cell fate determination.

Revisiting the famous farm foxes: A psychological perspective.

Five decades ago, Dmitry Belyaev, Lyudmila Trut, and colleagues began a now-famous experiment, selectively breeding foxes based on one criterion: perceived tame behavior. Over generations, the fox population changed in behavior (as predicted) but, intriguingly, also changed markedly in appearance-for example, many had wider mouths, curlier tails, different fur coloring, and floppy ears. These researchers concluded that the morphological changes that appeared in their foxes were a by-product of the researchers' selecting for genetic variants that are implicated both in behavior and in appearance. For decades, scientists have largely accepted this "shared genetic variants" interpretation to fully account for the co-occurrence of behavioral and morphological phenotypes in these foxes and in other domesticated animals. However, several decades of psychological research on human social cognition, human-canine interaction, and canine behavior strongly suggest that such an account may be incomplete. I forward a supplementary perspective, based on psychological research, that the covariation of appearance and behavior among these foxes may be partly an artifact of human psychological processes at play in selection. These processes include humans' tendency to infer individuals' traits based on their physical features; trait inferences, in turn, influence how humans treat those individuals. If accurate, this account bears on our understanding of these famous foxes, human-canine interactions, as well as humans' role in domestication.

Quantifying behavioral changes in territorial animals caused by sudden population declines.

Although territorial animals are able to maintain exclusive use of certain regions of space, movement data from neighboring individuals often suggest overlapping home ranges. To explain and unify these two aspects of animal space use, we use recently developed mechanistic models of collective animal movement. We apply our approach to a natural experiment on an urban red fox (Vulpes vulpes) population that underwent a rapid decline in population density due to a sarcoptic mange epizooty. By extracting details of movement and interaction strategies from location data, we show how foxes alter their behavior, taking advantage of sudden population-level changes by acquiring areas vacated due to neighbor mortality, while ensuring territory boundaries remain contiguous. The rate of territory border movement increased eightfold as the population declined and the foxes' response time to neighboring scent reduced by a third. By demonstrating how observed, fluctuating territorial patterns emerge from movements and interactions of individual animals, our results give the first data-validated, mechanistic explanation of the elastic disc hypothesis, proposed nearly 80 years ago.

Genetics of behavior in the silver fox.

The silver fox provides a rich resource for investigating the genetics of behavior, with strains developed by intensely selective breeding that display markedly different behavioral phenotypes. Until recently, however, the tools for conducting molecular genetic investigations in this species were very limited. In this review, the history of development of this resource and the tools to exploit it are described. Although the focus is on the genetics of domestication in the silver fox, there is a broader context. In particular, one expectation of the silver fox research is that it will be synergistic with studies in other species, including humans, to yield a more comprehensive understanding of the molecular mechanisms and evolution of a wider range of social cognitive behaviors.

Directional preference may enhance hunting accuracy in foraging foxes.

Red foxes hunting small animals show a specific behaviour known as 'mousing'. The fox jumps high, so that it surprises its prey from above. Hearing seems to be the primary sense for precise prey location in high vegetation or under snow where it cannot be detected with visual cues. A fox preparing for the jump displays a high degree of auditory attention. Foxes on the prowl tend to direct their jumps in a roughly north-eastern compass direction. When foxes are hunting in high vegetation and under snow cover, successful attacks are tightly clustered to the north, while attacks in other directions are largely unsuccessful. The direction of attacks was independent of time of day, season of the year, cloud cover and wind direction. We suggest that this directional preference represents a case of magnetic alignment and enhances the precision of hunting attacks.

Predator dietary response to prey density variation and consequences for cestode transmission.

The functional response of predators to prey density variations has previously been investigated in order to understand predation patterns. However, the consequences of functional response on parasite transmission remain largely unexplored. The rodents Microtus arvalis and Arvicola terrestris are the main prey of the red fox Vulpes vulpes in eastern France. These species are intermediate and definitive hosts of the cestode Echinococcus multilocularis. We explored the dietary and contamination responses of the red fox to variations in prey density. The dietary response differed between the two prey species: no response for M. arvalis and a type III-like (sigmoidal) response for A. terrestris that shows possible interference with M. arvalis. The fox contamination response followed a type II shape (asymptotic) for both species. We conclude that fox predation is species specific and E. multilocularis transmission is likely to be regulated by a complex combination of predation and immunologic factors. These results should provide a better understanding of the biological and ecological mechanisms involved in the transmission dynamics of trophically transmitted parasites when multiple hosts are involved. The relevance of the models of parasite transmission should be enhanced if non-linear patterns are taken into account.

Is alloparenting helpful for Mednyi Island arctic foxes, Alopex lagopus semenovi?

The Arctic Fox Alopex lagopus semenovi population on Mednyi Island is completely isolated and subsists largely by scavenging on seabird colonies, which have remained abundant and spatio-temporally predictable for many years. We compared population data at the beginning of 1976/1978 and some time after 1994-2005, finding an 85% decline in fox numbers due to disease, to assess the effect of population size on social structure. A total of 81 groups of known size and composition was observed during this 29-year period. Overall, helpers (usually non-lactating yearling females) occurred in 25.7% of groups, and in 32.4% of groups there were two or three lactating females. Female engagement in alloparental behaviour decreased, but not statistically significantly, after the decline in population density. Total food availability was apparently constant throughout the study period, and therefore, the amount available per individual was much higher later in the study. Both communally nursing females and helpers brought food and helped to guard the litter. However, the benefits of communal rearing were unclear. While cubs were left without guards significantly more rarely in the groups with an additional adult, the number of cubs weaned per lactating female was greater in groups with one (3.93 +/- 1.60), as opposed to two or three (3.06 +/- 0.92), lactating females. Survival of cubs to 1 year of age in the groups with two lactating females and/or with helpers was lower than that in the families with one lactating female without helpers (22.2% vs 32.2%). Fewer second-generation litters were born to foxes produced by composite families than to those produced by pairs. Reproductive adults producing by pairs had, on average, 1.23 (+/-1.72) second-generation litters. In groups that initially included additional adults, the average number of second-generation litters per reproductive female was 0.21 (+/-0.49) and 0.46 (+/-0.81) litters per male. Thus, according to three measures, increased group size had no apparent positive impact on reproductive success. The increased parental investment and enhanced guarding of the cubs in the larger families could be beneficial under conditions of high population density and a saturated biotope to which the island fox population was presumably adapted before the population crash in the late 1970s.

Living with roommates in a shared den: Spatial and temporal segregation among semifossorial mammals.

Positive interspecific interactions in animal communities (i.e. den sharing) have long been overlooked in animal ecology. The assessment of spatiotemporal overlap among species living within the same burrow system is paramount to explain their strategies of interspecific coexistence. We studied spatiotemporal behavioural patterns of coexistence among four den-sharing mammal species (i.e. the crested porcupine Hystrix cristata, the Eurasian badger Meles meles, the red fox Vulpes vulpes and the European pine marten Martes martes), inhabiting a hilly area of central Italy. Intensive camera trapping (September 2015-September 2018) was used to estimate the interspecific overlap of both temporal and spatial activity patterns for all species combinations. An extensive nocturnal temporal overlap was recorded among all the species, except the diurnal pine marten. However, crested porcupines were mostly active in the darkest nights, whereas bright moonlight enhanced the hunting success of the red fox. Activity of badgers was limited in bright nights only during cold months, when predation pressure and poaching risk were the highest. Crested porcupines avoided spatial sharing outside the den with both nocturnal carnivores, particularly during the winter, when its cubs are in the den. Overlap in ranging areas and activity rhythms between the red fox and the Eurasian badger may be promoted by a remarkable food niche partitioning. Conversely, spatiotemporal overlap between red foxes and pine martens suggested a significant interspecific spatial partitioning, due to the overlap in feeding habits. Den-sharing represents a form of positive interspecific interaction which may limit energy waste and increase local species diversity and densities. Species using the same burrow system may show both spatial and temporal niche partitioning throughout the year, thus allowing a non-competitive coexistence.

Habitat selection and diurnal refugia of gray foxes in southwestern Georgia, USA.

Understanding habitat selection of gray foxes (Urocyon cinereoargenteus) is essential to evaluate their potential response to changes in land use and predator communities. Few studies have evaluated temporal habitat selection or explicitly identified habitats used by gray foxes for diurnal refugia. We used GPS collars to obtain location data for 34 gray foxes (20 males and 14 females) from February 2014 to December 2015 to evaluate temporal (seasonal and diel) habitat selection and selection of diurnal refugia in southwestern Georgia, USA. We analyzed habitat selection at 2 levels, selection of a core area within the home range and selection of locations within the home range. Habitat selection was non-random (P < 0.001) but consistent among seasons, between day and night, and between sexes (P > 0.05). Hardwoods, human use (i.e., areas associated with regular human activity such as buildings, lawns, parking areas, etc.), and roads were selected (P < 0.05), whereas pine dominated stands were used randomly (P > 0.05). Selection of habitats for diurnal refugia did not vary seasonally or by sex (P > 0.05), with foxes selecting (P < 0.05) areas near hardwood forests, roads, agriculture, human use, pastures/food plots, and shrub scrub habitats. Gray foxes were observed on the ground while resting, and we found no evidence of gray foxes diurnally resting in trees. Our results suggest that on our study area, gray foxes are an edge species that prefer forests with a hardwood component in areas near human use and roads.

Evidence for the involvement of central serotonin in mechanism of domestication of silver foxes.

Silver foxes selected for more than 30 years for tame behavior and displaying no defensive reaction to human contact were shown to have a higher serotonin level in midbrain and hypothalamus, and a higher 5-hydroxyindole acetic acid (5-HIAA) content in midbrain, hypothalamus and hippocampus in comparison to nonselected wild silver foxes bred in captivity over the same time span. Tryptophan hydroxylase (TPH) activity in midbrain and hypothalamus in domesticated foxes was increased as compared with their aggressive/defensive counterparts. Monoamine oxidase type A (MAO A) activity was was decreased with an increased Km and unchanged Vmax in domesticated foxes. No changes in specific [3H]ketanserin or [3H]8-OH-DPAT binding in frontal cortex was revealed. A reduced density (Bmax) of 5HT1A receptors in hypothalamic membranes in domesticated foxes was shown. It is suggested that the brain serotonergic system is involved in the mechanism of domestication converting wild aggressive/defensive animals into tame ones.

Gray fox response to baits and attractants for oral rabies vaccination.

Rabies is a widespread zoonosis that recently reached epidemic proportions in gray foxes (Urocyon cinereoargenteus) in central Texas. The objectives of this study were to determine bait and attractant preferences among captive gray foxes, to determine the behavioral responses of gray foxes to selected bait-attractant combinations, and to evaluate baits as a delivery mechanism of oral rabies vaccines. Trials were conducted to determine bait preferences of captive gray foxes to selected baits and attractants. Tested baits consisted of a polymer-bound cube made of either dog food meal or fish meal, a polymer-bound cylinder made of dog food meal, and a wax-lard cake that was enhanced with marshmallow or chicken flavoring. Attractants were additives to baits that exuded sweet, sulfurous, fruity, fatty, cheesy, honey, and fishy odors and flavors. Captive gray foxes (n = 31) exhibited a preference for marshmallow wax cakes and polymer dog food baits with a lard interior and granulated sugar exterior. However, gray foxes exhibited chewing behaviors consistent with ingesting an oral vaccine only with the wax cake baits.

The bat-eared fox: a prime candidate for rabies vector?

Bat-eared foxes, Otocyon megalotis, are small (3-5 kg), primarily insectivorous carnivores widespread in the more arid areas of southern and East Africa. For many months of the year they live in nuclear family groups, members of which frequently indulge in affiliative behaviour such as play, allogrooming, and huddling. Physical contact between individuals in any particular group is thus common. In addition, groups are non-territorial and intermingle freely at times when exploiting food-rich patches of clumped prey, e.g. individuals foraging for harvester termites, Hodotermes mossambicus.

Bat-eared fox behavioural ecology and the incidence of rabies in the Serengeti National Park.

This paper provides a brief introduction into some aspects of bat-eared fox biology and social organization that is important to understanding rabies transmission and disease management in susceptible wildlife species (Macdonald 1980; 1993). A detailed description of the effects of two rabies outbreaks on a population of known individuals in the Serengeti National Park is given, Inter- and intrasexual differences in adult mortality rates are reported and discussed.

Effects of handling and physical restraint on rectal temperature, cortisol, glucose and leucocyte counts in the silver fox (Vulpes vulpes).

The present paper describes the effects of handling and one hour of physical restraint on rectal temperature (Trec), plasma cortisol, plasma glucose and leucocyte counts in six 8-months old silver fox vixens (Vulpes vulpes). Mean Trec in silver foxes 5 min after capture was 40.1 degrees C and increased during restraint, showing a maximum of 40.8 degrees C at 30 min thereafter. Supplementary, deep body temperature (Tb) was recorded with surgically implanted biotelemetry devices in 6 adult silver fox vixens kept isolated from environmental disturbances in a barn. Mean Tb in these foxes ranged between 38.0-38.4 degrees C, showing a diurnal variation and being at the lowest between 0700-1600 hour. When a person approached a fox and was present for 5 min, Tb increased rapidly. The results indicated that a stress-induced hyperthermia (SIH) was evoked rapidly within the first registration at 5 min after capture, and that this response continued during one hour of physical restraint. Plasma glucose and plasma cortisol levels increased during one hour of physical restraint, whereas numbers of lymphocytes, total white blood cell counts, and total granulocytes decreased. Furthermore, previously reported base levels of plasma cortisol and plasma glucose were exceeded. The results indicate that the hypothalamic-pituitary-adrenal (HPA) axis and the sympathoadrenal medullary (SAM) system were activated within 5 min of handling and restraint. Furthermore, hyperthermia is a promising indicator of acute stress in silver foxes.

Learning interspecific communicative responses in Pampas foxes (Lycalopex gymnocercus).

Domestic dogs show remarkable communicative abilities in their interaction with people. These skills maybe explained by the interaction between the domestication process and learning experiences during ontogeny. Studies carried out on other species of canids, which have not been domesticated are relevant to this topic. The purpose of this article is to study the effect of instrumental learning on captive Pampas foxes' (Lycalopex gymnocercus) communicative responses to humans. Seven foxes were tested in a conflict situation involving food within sight but out of their reach. In these situations dogs typically gaze at the human face to ask for food. In Study 1, there was an increase in gaze duration as a consequence of reinforcement and a decrease during extinction, when animals did not receive any more food. In Study 2, all of the four foxes tested successfully followed proximal pointing gesture to find hidden food. When a distal pointing cue was given, three out of four followed it in the first session and one in the second session. These results are consistent with those previously found in dogs, and suggest that learning experiences allow the development of communicative skills, even in not domesticated canid species.

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.

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.