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.     

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.     

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.     

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.     

Expression of the DNA methyltransferase genes in silver foxes experimentally selected for domestication

Animal domestication is a model of a rapid evolutionary process. In experimental fox domestication, the time required for the emergence and fixation of specific evolutionary changes was reduced from thousands to tens of years, compared to historical domestication. Tame foxes were obtained by extreme selective breeding for emotionally positive response toward humans. Unselected foxes, as well as foxes bred for enhanced aggressiveness to humans were used as control. Epigenetic regulation of gene expression is considered as one of the possible mechanisms of rapid evolution. In this study, expression of DNA methyltransferase genes, DNMT1 and DNMT3A, was investigated. It was demonstrated that, in tame foxes, the level of DNMT3A gene expression in the prefrontal cortex, hippocampus, and spleen was increased by more than 2 times in comparison with aggressive and unselected foxes. At the same time, the DNMT1 expression level did not differ among the studied groups of animals. A possible reason for the differences found in the DNMT3A expression could be the changes in the level and metabolism of methionine, which serves as a donor of methyl groups during DNA methylation. However, this study showed that there were no differences in the serum methionine levels between tame, unselected, and aggressive foxes. Thus, the data support the hypothesis that selection for positive emotional response toward humans affected the DNA methylation machinery.     

Genotyping-By-Sequencing (GBS) Detects Genetic Structure and Confirms Behavioral QTL in Tame and Aggressive Foxes (Vulpes vulpes)

The silver fox (Vulpes vulpes) offers a novel model for studying the genetics of social behavior and animal domestication. Selection of foxes, separately, for tame and for aggressive behavior has yielded two strains with markedly different, genetically determined, behavioral phenotypes. Tame strain foxes are eager to establish human contact while foxes from the aggressive strain are aggressive and difficult to handle. These strains have been maintained as separate outbred lines for over 40 generations but their genetic structure has not been previously investigated. We applied a genotyping-by-sequencing (GBS) approach to provide insights into the genetic composition of these fox populations. Sequence analysis of EcoT22I genomic libraries of tame and aggressive foxes identified 48,294 high quality SNPs. Population structure analysis revealed genetic divergence between the two strains and more diversity in the aggressive strain than in the tame one. Significant differences in allele frequency between the strains were identified for 68 SNPs. Three of these SNPs were located on fox chromosome 14 within an interval of a previously identified behavioral QTL, further supporting the importance of this region for behavior. The GBS SNP data confirmed that significant genetic diversity has been preserved in both fox populations despite many years of selective breeding. Analysis of SNP allele frequencies in the two populations identified several regions of genetic divergence between the tame and aggressive foxes, some of which may represent targets of selection for behavior. The GBS protocol used in this study significantly expanded genomic resources for the fox, and can be adapted for SNP discovery and genotyping in other canid species.     

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.     

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.     

菲律宾Boracay岛和Mambukal岛三种共栖狐蝠对人类活动的行为和激素反应

栖息地丧失和捕猎导致许多大型狐蝠濒危。尽管在东半球热带地区已经禁止捕猎和采伐,狐蝠的数量仍然在下降。既能维护当地居民利益又能保护狐蝠的折衷对策是生态旅游。然而,人类活动对狐蝠的影响还是未知的。菲律宾Boracay和Mambukal都是旅游区,前者游人少而稳定,后者游人密集且变异较大。我们用非损伤取样法研究了这两个旅游区三种狐蝠的生理紧张情况。在Mambukal,当狐蝠外出采食时,采集狐蝠的粪样,实验室分析粪样肾上腺皮质激素代谢物(GCM)浓度。我们观察记录了紧张反应等一些行为,同时记录了环境因素和人类活动情况。结果表明狐蝠已经习惯了游人的活动,表现在:(1)我们发现两个旅游区游人数量和活动强度差异显著,但是两地狐蝠的行为没有明显的差异;并且在有干扰和无干扰的日期之间,狐蝠的行为也无显著差异;两个旅游区的狐蝠行为表达一致;(2)各种行为与测定的粪样GCM浓度都不相关;(3)尽管在不同研究地点人类活动变异很大,我们发现人类活动并未影响粪样GCM浓度;不过,栖息在狐蝠群中心位置个体的粪样GCM浓度低于在群外围个体的GCM浓度;(4)一些环境因素(如干扰以及与栖息群的距离)影响狐蝠一些行为(如不安、身体护理和哈欠)的表达。如果干扰没有造成狐蝠紧张反应,那么生态旅游将不失为一种保护濒危狐蝠栖息地的理想方案。不过,我们还应认识到,人类干扰对狐蝠行为的影响可能比本研究观察到的更加复杂。因此,对于保护濒危狐蝠,时刻保持干扰最小是最好的选择。     

Reproductive potential of male silver foxes Vulpes vulpes after long selection for the domesticated behavior type

Age peculiarities of reproductive activity and fertility during the reproductive season as well as the hormonal and the testis spermatogenic function were studied in silver foxes Vulpes vulpes from the population selected for a long time for domesticated behavior. It has been established that during the first reproductive season the male sexually activity (the coupled females’ number) was reduced as compared with subsequent seasons, and about one third of the males were not coupled at all with females; however, the young (one-year old) males did not differ from adults by the testis weight, ejaculate spermatozoid number, and the fraction of abnormal spermatozoids. Comparison of indexes of spermatogenesis and the testicular hormonal function in the young males with a decreased and “normal” sexual activity did not reveal any statistically significant differences. It is suggested that the decreased (or absent) sexual activity in young silver fox males can be a response of the population to the human-created environment.     

Genetic polymorphism of plasma α1B-glycoprotein and transferrin in arctic and silver foxes

Plasma samples of 235 foxes from 38 complete families (14 of arctic foxes, 21 of silver foxes and 3 with arctic x silver fox hybrid offspring) were analysed by one-dimensional horizontal polyacrylamide gel electrophoresis (PAGE) pH 9.0 followed by general-protein staining of gels. A major postalbumin of fox plasma was identified as alpha 1B-glycoprotein (alpha 1B) by using immunoblotting with antiser m specific to human or pig plasma alpha 1B. Four codominant, autosomal alleles of alpha 1B were found in arctic foxes. Two transferrin (TF) alleles (TfF, TfS) were observed in arctic foxes and two (TfD, Tff) in silver foxes; the TF F type of both of the fox species showed identical electrophoretic mobilities. The arctic foxes showed a high degree of polymorphism for both TF and alpha 1B. The silver foxes showed a scarce polymorphism of TF and were monomorphic for alpha 1B. The arctic fox, silver fox and their hybrids could be clearly differentiated from one another by their plasma protein patterns obtained by the PAGE method.     

Behavioral effects of bidirectional selection for behavior towards human in virgin and lactate Norway rats

Although numerous studies have demonstrated strong differences in behavioral, hormonal and neurobiological characteristics between male rats selected for elimination (tame) and enhancement (aggressive) of aggressiveness towards humans, few studies have examined changes in female behavior under this selection. The objective of the current work was to evaluate the effects of bidirectional selection for aggressiveness towards humans on behavioral profiles of virgin and lactating rats compared with the behavior in tame, aggressive and unselected (wild-type) females. The behavior of virgin females was studied using the light-dark box, the startle response test and the modified glove test. Tame females were less anxious and more tolerant towards humans than unselected and aggressive rats. Principal component analysis of all behavioral parameters produced three independent factors, explaining 66.37% of the total variability. The measures of behavior towards humans and the measures of anxiety mainly loaded on PC1 (first principal component) which separated the tame females from the unselected and aggressive ones. These data suggest the genetic correlation between the selected behavior towards humans and anxiety-related behavior in virgin rats. No significant effect of line was found for PC2 scores, associated with risk assessment behavior. Measurements of freezing behavior mainly loaded on PC3, and this component separated rats of different genetic groups from each other. The behavior of lactating rats was studied in maternal defense and pup retrieval tests. Females of selected lines did not significantly differ in behavioral measurements of these tests and were characterized by higher maternal motivation than unselected rats. It is suggested that long-term breeding of tame and aggressive rats in captivity has reduced the threshold for maternal behavior.     

Development of Auditory-Vocal Perceptual Skills in Songbirds

Songbirds are one of the few groups of animals that learn the sounds used for vocal communication during development. Like humans, songbirds memorize vocal sounds based on auditory experience with vocalizations of adult “tutors”, and then use auditory feedback of self-produced vocalizations to gradually match their motor output to the memory of tutor sounds. In humans, investigations of early vocal learning have focused mainly on perceptual skills of infants, whereas studies of songbirds have focused on measures of vocal production. In order to fully exploit songbirds as a model for human speech, understand the neural basis of learned vocal behavior, and investigate links between vocal perception and production, studies of songbirds must examine both behavioral measures of perception and neural measures of discrimination during development. Here we used behavioral and electrophysiological assays of the ability of songbirds to distinguish vocal calls of varying frequencies at different stages of vocal learning. The results show that neural tuning in auditory cortex mirrors behavioral improvements in the ability to make perceptual distinctions of vocal calls as birds are engaged in vocal learning. Thus, separate measures of neural discrimination and behavioral perception yielded highly similar trends during the course of vocal development. The timing of this improvement in the ability to distinguish vocal sounds correlates with our previous work showing substantial refinement of axonal connectivity in cortico-basal ganglia pathways necessary for vocal learning.     

Identifying Hendra virus diversity in pteropid bats

Hendra virus (HeV) causes a zoonotic disease with high mortality that is transmitted to humans from bats of the genus Pteropus (flying foxes) via an intermediary equine host. Factors promoting spillover from bats to horses are uncertain at this time, but plausibly encompass host and/or agent and/or environmental factors. There is a lack of HeV sequence information derived from the natural bat host, as previously sequences have only been obtained from horses or humans following spillover events. In order to obtain an insight into possible variants of HeV circulating in flying foxes, collection of urine was undertaken in multiple flying fox roosts in Queensland, Australia. HeV was found to be geographically widespread in flying foxes with a number of HeV variants circulating at the one time at multiple locations, while at times the same variant was found circulating at disparate locations. Sequence diversity within variants allowed differentiation on the basis of nucleotide changes, and hypervariable regions in the genome were identified that could be used to differentiate circulating variants. Further, during the study, HeV was isolated from the urine of flying foxes on four occasions from three different locations. The data indicates that spillover events do not correlate with particular HeV isolates, suggesting that host and/or environmental factors are the primary determinants of bat-horse spillover. Thus future spillover events are likely to occur, and there is an on-going need for effective risk management strategies for both human and animal health.     

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     

Morphofunctional status of the adrenal cortex in female silver foxes and the effect of domestication and photoperiodic conditions

Studies on 7-day-old and 8-month-old female silver foxes indicate that additional photostimulation affects to a various extent morphological and functional condition of the adrenal cortex in animals selected and unselected for the domestication type of behaviour. In relatively wild foxes, additional illumination stimulated the activity of the reticular zone, whereas in domesticated animals the same photoperiod increased the activity in the fascicular zone. It is suggested that selection of silver foxes for the domestication type of behaviour affects the sensitivity of the adrenals to external illumination.     

Cervids with different vocal behavior demonstrate different viscoelastic properties of their vocal folds

The authors test the hypothesis that vocal fold morphology and biomechanical properties covary with species‐specific vocal function. They investigate mule deer (Odocoileus hemionus) vocal folds, building on, and extending data on a related cervid, the Rocky Mountain elk (Cervus elaphus nelsoni). The mule deer, in contrast to the elk, is a species with relatively little vocal activity in adult animals. Mule deer and elk vocal folds show the typical three components of the mammalian vocal fold (epithelium, lamina propria and thyroarytenoid muscle). The vocal fold epithelium and the lamina propria were investigated in two sets of tensile tests. First, creep rupture tests demonstrated that ultimate stress in mule deer lamina propria is of the same magnitude as in elk. Second, cyclic loading tests revealed similar elastic moduli for the vocal fold epithelium in mule deer and elk. The elastic modulus of the lamina propria is also similar between the two species in the low‐strain region, but differs at strains larger than 0.3. Sex differences in the stress–strain response, which have been reported for elk and human vocal folds, were not found for mule deer vocal folds. The laminae propriae in mule deer and elk vocal folds are comparatively large. In general, a thick and uniformly stiff lamina propria does not self‐oscillate well, even when high subglottic pressure is applied. If the less stiff vocal fold seen in elk is associated with a differentiated lamina propria it would allow the vocal fold to vibrate at high tension and high subglottic pressure. The results of this study support the hypothesis that viscoelastic properties of vocal folds varies with function and vocal behavior. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Rabid foxes, rabid raccoons, and the odds of a human bite exposure, New York State, 1999-2007

Anecdotal evidence suggests that rabid foxes are more likely to attack humans than are other rabid terrestrial animals. To examine this issue, we analyzed rabies surveillance data (1999-2007) maintained by the New York State Department of Health. Compared to rabid raccoons (Procyon lotor), foxes infected with raccoon variant rabies were more likely to bite during a human exposure incident (P<0.01). Additionally, rabid gray foxes (Urocyon cinereoargenteus) were significantly more likely to bite a human than were rabid red foxes (Vulpes vulpes; P<0.01). Animal control personnel and others who handle wildlife should be educated about the increased risk of bite exposure when dealing with potentially rabid foxes.     

Mitochondrial Genomes Suggest Rapid Evolution of Dwarf California Channel Islands Foxes (Urocyon littoralis)

Island endemics are typically differentiated from their mainland progenitors in behavior, morphology, and genetics, often resulting from long-term evolutionary change. To examine mechanisms for the origins of island endemism, we present a phylogeographic analysis of whole mitochondrial genomes from the endangered island fox (Urocyon littoralis), endemic to California’s Channel Islands, and mainland gray foxes (U. cinereoargenteus). Previous genetic studies suggested that foxes first appeared on the islands >16,000 years ago, before human arrival (~13,000 cal BP), while archaeological and paleontological data supported a colonization >7000 cal BP. Our results are consistent with initial fox colonization of the northern islands probably by rafting or human introduction ~9200–7100 years ago, followed quickly by human translocation of foxes from the northern to southern Channel Islands. Mitogenomes indicate that island foxes are monophyletic and most closely related to gray foxes from northern California that likely experienced a Holocene climate-induced range shift. Our data document rapid morphological evolution of island foxes (in ~2000 years or less). Despite evidence for bottlenecks, island foxes have generated and maintained multiple mitochondrial haplotypes. This study highlights the intertwined evolutionary history of island foxes and humans, and illustrates a new approach for investigating the evolutionary histories of other island endemics.