Rhesus monkeys correctly read the goal-relevant gestures of a human agent

When humans point, they reveal to others their underlying intent to communicate about some distant goal. A controversy has recently emerged based on a broad set of comparative and phylogenetically relevant data. In particular, whereas chimpanzees (Pan troglodytes) have difficulty in using human-generated communicative gestures and actions such as pointing and placing symbolic markers to find hidden rewards, domesticated dogs (Canis familiaris) and silver foxes (Urocyon cinereoargenteus) readily use such gestures and markers. These comparative data have led to the hypothesis that the capacity to infer communicative intent in dogs and foxes has evolved as a result of human domestication. Though this hypothesis has met with challenges, due in part to studies of non-domesticated, non-primate animals, there remains the fundamental question of why our closest living relatives, the chimpanzees, together with other non-human primates, generally fail to make inferences about a target goal of an agent's communicative intent. Here, we add an important wrinkle to this phylogenetic pattern by showing that free-ranging rhesus monkeys (Macaca mulatta) draw correct inferences about the goals of a human agent, using a suite of communicative gestures to locate previously concealed food. Though domestication and human enculturation may play a significant role in tuning up the capacity to infer intentions from communicative gestures, these factors are not necessary.     

Sex ratio in silver foxes: effects of domestication and the star gene

The course of changes in secondary sex ratio (proportion of males at birth) in silver foxes bred at the fur farm of this Institute was analyzed. Data collected over several years of breeding of a domesticated (experimental) population selected for amenability to domestication and of a commercial (control) were compared. A tendency to increase in secondary sex ratio was demonstrated in both populations. However, the proportion of males at birth was higher in domestic foxes. This proportion, calculated from the combined data for 1978–1993, was 0.538±0.005 and 0.511±0.007 in the selected and commercial populations, respectively. The minimal departure of the observed sex ratio from 0.5 was demonstrated for litters with five pups, which is close to the average litter size in fox populations. The proportion of males increases with both increasing and decreasing litter size. An analysis of secondary sex ratio with respect to maternal age revealed a minimal departure of sex ratio from the expected in offspring from foxes of optimal reproductive age (2–4 years). An effect of the autosomal semidominant coat color mutation star on male excess at birth was also found: secondary sex ratio was higher (0.583±0.015) in offspring of mothers heterozygous for the star mutation than from standard types of the domesticated population. The increase in secondary sex ratio in the analyzed fox populations is viewed as a correlated response to selection for domestication. The hormonal mechanisms mediating the effects of both this selection and the star mutation on sex ratio at birth are discussed.     

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.     

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.     

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.     

A marker set for construction of a genetic map of the silver fox (Vulpes vulpes)

The silver fox, a variant of the red fox (Vulpes vulpes), is a close relative of the dog (Canis familiaris). Cytogenetic differences and similarities between these species are well understood, but their genomic organizations have not been compared at higher resolution. Differences in their behavior also remain unexplained. Two silver fox strains demonstrating markedly different behavior have been generated at the Institute of Cytology and Genetics of the Russian Academy of Sciences. Foxes selected for tameness are friendly, like domestic dogs, while foxes selected for aggression resist human contact. To refine our understanding of the comparative genomic organization of dogs and foxes, and enable a study of the genetic basis of behavior in these fox strains, we need a meiotic linkage map of the fox. Towards this goal we generated a primary set of fox microsatellite markers. Four hundred canine microsatellites, evenly distributed throughout the canine genome, have been identified that amplify robustly from fox DNA. Polymorphism information content (PIC) values were calculated for a representative subset of these markers and population inbreeding coefficients were determined for tame and aggressive foxes. To begin to identify fox-specific single nucleotide polymorphisms (SNPs) in genes involved in the neurobiology of behavior, fox and dog orthologs of serotonin 5-HT1A and 5-HT1B receptor genes have been cloned. Sequence comparison of these genes from tame and aggressive foxes reveal several SNPs. The close relationship of the fox and dog enables canine genomic tools to be utilized in developing a fox meiotic map and mapping behavioral traits in the fox.     

Exclusion by interference competition? The relationship between red and arctic foxes

The distribution of many predators may be limited by interactions with larger predator species. The arctic fox in mainland Europe is endangered, while the red fox is increasing its range in the north. It has been suggested that the southern distribution limit of the arctic fox is determined by interspecific competition with the red fox. This has been criticised, on the basis that the species co-exist on a regional scale. However, if the larger red fox is superior and interspecific competition important, the arctic fox should avoid close contact, especially during the breeding season. Consequently, the distribution of breeding dens for the two species would be segregated on a much smaller spatial and temporal scale, in areas where they are sympatric. We tested this hypothesis by analysing den use of reproducing arctic and red foxes over 9 years in Sweden. High quality dens were inhabited by reproducing arctic foxes more often when no red foxes bred in the vicinity. Furthermore, in two out of three cases when arctic foxes did reproduce near red foxes, juveniles were killed by red foxes. We also found that breeding arctic foxes occupied dens at higher altitudes than red foxes did. In a large-scale field experiment, red foxes were removed, but the results were not conclusive. However, we conclude that on the scale of individual territories, arctic foxes avoid areas with red foxes. Through interspecific interference competition, the red fox might thus be excluding the arctic fox from breeding in low altitude habitat, which is most important in years when food abundance is limited and competition is most fierce. With high altitude refuges being less suitable, even small-scale behavioural effects could scale up to significant effects at the population level.     

Animal evolution during domestication: the domesticated fox as a model

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.     

Rabies and canine distemper in an arctic fox population in Alaska

Two oil field workers were attacked by a rabid arctic fox (Alopex lagopus) in the Prudhoe Bay oil field (Alaska, USA) prompting officials to reduce the local fox population. Ninety-nine foxes were killed during winter 1994. We tested foxes for prevalence of rabies and canine distemper. Exposure to rabies was detected in five of 99 foxes. Of the five, only one fox had rabies virus in neural tissue as determined by the direct fluorescent antibody test. The other four foxes had been exposed to rabies, but had apparently produced antibodies and did not have an active infection. No evidence of canine distemper was detected as determined by the absence of distemper antibodies in serum and distemper virus in neural tissue.     

Possible contemporary evolution in an endangered species, the Santa Cruz Island fox

An ability to mount rapid evolutionary responses to environmental change may be necessary for species persistence in a human-dominated world. We present evidence of the possibility of such contemporary evolution in the anti-predator behaviour of the critically endangered Santa Cruz Island fox Urocyon littoralis . In 1994, golden eagles colonized Santa Cruz Island, CA and devastated the predator-naïve, endemic island fox population by 95% within 10 years. In 1992, just before the arrival of golden eagles, foxes showed substantial diurnal activity, but diurnal activity was 37.0% lower in 2003–2007, after golden eagle colonization; concurrently, overall activity declined and nocturnal activity increased. Moreover, on nearby Santa Catalina Island, where golden eagles were absent but where the fox population recently crashed due to a disease epidemic, remaining foxes were significantly more diurnally active than were those on Santa Cruz Island. The weight of evidence suggests that the change in activity pattern was a response to predation, not to low population density, and that this was probably a heritable rather than a learned behavioural trait. This behavioural change may allow for prolonged island fox persistence, but also potentially represents a loss of behavioural diversity in fox populations.     

Survival and Cause-Specific Mortality of Corsac and Red Foxes in Mongolia

ABSTRACT The corsac fox (Vulpes corsac) and red fox (Vulpes vulpes) range widely across northern and central Asia and may be declining in many regions due to overhunting and other causes. However, details of the fundamental causes of survival and mortality of both species remain largely unquantified, but may be crucial for understanding interspecific relationships and developing effective conservation actions. We studied a radiomarked population of sympatric corsac and red foxes in central Mongolia to quantify survival and cause-specific mortality rates from April 2005 to April 2007. Survival probability was 0.34 for corsacs (n = 18) and 0.46 for red foxes (n = 17) and did not vary by year within or between each species. Among both foxes, mortality occurred mainly from hunting by humans, but also from predation by larger canids and unknown causes. Our results suggest that illegal human hunting represents the principal source of mortality for both species and that a recently initiated ranger patrol program in the study area did not affect fox survival. As such, more stringent protective measures will likely be necessary to halt declines of both foxes. Our results also suggest that interference competition occurs between species as red foxes killed but did not consume corsacs. Our results will be useful for developing science-based management strategies to protect foxes in Mongolia, and in understanding the competitive relationships between them.     

Evaluating the self‐domestication hypothesis of human evolution

“Self‐domestication” has been invoked to understand important aspects of human evolution, integrating physiological, behavioral, and morphological information in a novel way. It proposes that selection for reduced aggression on animals undergoing domestication provides a model for selection favoring prosocial behaviors in humans and for a set of seemingly independent features, which arose as a result of developmental correlation. We review the history of the idea and examine patterns of domestication. A lack of empirical studies on evolutionary rates and variation thwarts meaningful comparison with domestication. The neural crest hypothesis for domestication has great explanatory power but it is difficult to test. We suggest a scenario in which the morphological byproducts of domestication can act as an honest signal of reduced xenophobia. Future studies should test if alternative explanations for the features deemed to result from self‐domestication are mutually exclusive and generate data to test predictions of these hypotheses.     

Adapting to the human world: Dogs’ responsiveness to our social cues

Dogs are more skilful than a host of other species at tasks which require they respond to human communicative gestures in order to locate hidden food. Four basic interpretations for this proficiency surface from distilling the research findings. One possibility is that dogs simply have more opportunity than other species to learn to be responsive to human social cues. A different analysis suggests that the domestication process provided an opening for dogs to apply general cognitive problem-solving skills to a novel social niche. Some researchers go beyond this account and propose that dogs’ co-evolution with humans equipped them with a theory of mind for social exchanges. Finally, a more prudent approach suggests that sensitivity to the behaviours of both humans and conspecifics would be particularly advantageous for a social scavenger like the dog. A predisposition to attend to human actions allows for rapid early learning of the association between gestures and the availability of food.     

The evolution of population stability as a by-product of life-history evolution

Proposed mechanisms for the evolution of population stability include group selection through longterm persistence, individual selection acting directly on stability determining the demographic parameters, and the evolution of stability as a by-product of life-history evolution. None of these hypotheses currently has clear empirical support. Using two sets of Drosophila melanogaster populations, we provide experimental evidence of stability evolving as a correlated response to selection on traits not directly related to demography. Four populations (FEJs) were selected for faster development and early reproduction for 125 generations, and the other four (JBs) were ancestral controls. All FEJ and JB populations have been maintained on discrete generations at moderate density, thus eliminating differential selection on stability determining demographic parameters. We derived eight small populations from each FEJ and JB population, and subjected four small populations each to either stabilizing or destabilizing food regimes. Census data on these 64 small populations over 20 generations clearly showed that the FEJ populations have significantly less temporal fluctuations in their numbers in both food regimes compared to their controls. This greater stability of the FEJ populations is probably a by-product of the evolution of reduced fecundity and pre-adult survivorship, as a correlated response to selection for rapid development.     

On the origin of a domesticated species: Identifying the parent population of Russian silver foxes (Vulpes vulpes)

The foxes at Novosibirsk, Russia, are the only population of domesticated foxes in the world. These domesticated foxes originated from farm-bred silver foxes (Vulpes vulpes), whose genetic source is unknown. In this study we examined the origin of the domesticated strain of foxes and two other farm-bred fox populations (aggressive and unselected) maintained in Novosibirsk. To identify the phylogenetic origin of these populations we sequenced two regions of mtDNA, cytochrome b and D-loop, from 24 Novosibirsk foxes (8 foxes from each population) and compared them with corresponding sequences of native red foxes from Europe, Asia, Alaska and Western Canada, Eastern Canada, and the Western Mountains of the USA. We identified seven cytochrome b - D-loop haplotypes in Novosibirsk populations, four of which were previously observed in Eastern North America. The three remaining haplotypes differed by one or two base change from the most common haplotype in Eastern Canada. Φ(ST) analysis showed significant differentiation between Novosibirsk populations and red fox populations from all geographic regions except Eastern Canada. No haplotypes of Eurasian origin were identified in the Novosibirsk populations. These results are consistent with historical records indicating that the original breeding stock of farm-bred foxes originated from Prince Edward Island, Canada. Mitochondrial DNA data together with historical records indicate two stages in the selection of domesticated foxes: the first includes captive breeding for ~50 years with unconscious selection for behaviour; the second corresponds to over 50 further years of intensive selection for tame behaviour.     

Did ‘precautionary’ 1080 baiting have a realistic potential to eradicate Red Fox (Vulpes vulpes) in Tasmania without in situ monitoring data?

Anecdotal reports in 2001 suggested that the European Red Fox (Vulpes vulpes) had been deliberately released in Tasmania and thereafter an eradication programme using buried fluoroacetic acid (1080) baits was believed to be a necessary precautionary action until mid‐2013. Prerequisites for the successful eradication of foxes relate to the scale of the undertaking and the ability to collect in situ data such as the distribution and abundance of the target population and measures of the efficacy of the control technique. Previously, 1080 baiting has demonstrated only limited potential as a fox eradication technique on islands when used on a scale between 685 and 2141 times smaller than Tasmania. In the absence of empirical monitoring data confirming the distribution or abundance of extant foxes, buried baiting was targeted to specific landscapes believed to be preferred by foxes. No empirical data was collected concerning the in situ effectiveness of baiting in Tasmania, yet an a priori assumption of lethal efficacy was extrapolated from four heterogeneous mainland studies to suggest that foxes would have only a 0.23 probability of surviving each bait treatment. We show that these studies were unrepresentative of Tasmanian baiting methods used and influenced by imprecise fox population surveys and misreported data. Overall, in the absence of key population monitoring and efficacy data, the ‘precautionary’ baiting strategy adopted did not have a realistic potential to eradicate fox incursions in Tasmania, nor is it an appropriate risk management strategy for other large offshore Australian islands. Contingency plans to counter fox incursions on offshore islands must address the currently inadequate technical capacity to reliably detect and monitor low‐density fox populations, which is an essential component of successful fox eradication.     

Distribution, habitat utilization and age structure of a suburban fox (Vulpes vulpes) population

The occurrence of wild foxes in suburbia is discussed. It is shown that in London breeding populations of foxes are found 5 km from the city centre, and in the last 3 years foxes have been recorded in the very centre of the city. The fox population in London is shown to be heavily dependent on residential habitats for both daytime harbourage and when selecting sites for natal earths. The fox population is unevenly distributed in London, with a marked clumping of the adult population during most of the year. The age structure of the population is presented, and these data are compared with data for other canid populations. Conclusions are drawn as to the effects of conventional control techniques on the age structure of a fox population.